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Proc Natl Acad Sci U S A , IF:11.205 , 2024 Apr , V121 (18) : Pe2322751121 doi: 10.1073/pnas.2322751121

Organ-delimited gene regulatory networks provide high accuracy in candidate transcription factor selection across diverse processes.

Ranjan, Rajeev and Srijan, Sonali and Balekuttira, Somaiah and Agarwal, Tina and Ramey, Melissa and Dobbins, Madison and Kuhn, Rachel and Wang, Xiaojin and Hudson, Karen and Li, Ying and Varala, Kranthi

Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907.; Center for Plant Biology, Purdue University, West Lafayette, IN 47907.; United States Department of Agriculture-Agricultural Research Service Crop Production and Pest Control Research Unit, West Lafayette, IN 47907.

Organ-specific gene expression datasets that include hundreds to thousands of experiments allow the reconstruction of organ-level gene regulatory networks (GRNs). However, creating such datasets is greatly hampered by the requirements of extensive and tedious manual curation. Here, we trained a supervised classification model that can accurately classify the organ-of-origin for a plant transcriptome. This K-Nearest Neighbor-based multiclass classifier was used to create organ-specific gene expression datasets for the leaf, root, shoot, flower, and seed in Arabidopsis thaliana. A GRN inference approach was used to determine the: i. influential transcription factors (TFs) in each organ and, ii. most influential TFs for specific biological processes in that organ. These genome-wide, organ-delimited GRNs (OD-GRNs), recalled many known regulators of organ development and processes operating in those organs. Importantly, many previously unknown TF regulators were uncovered as potential regulators of these processes. As a proof-of-concept, we focused on experimentally validating the predicted TF regulators of lipid biosynthesis in seeds, an important food and biofuel trait. Of the top 20 predicted TFs, eight are known regulators of seed oil content, e.g., WRI1, LEC1, FUS3. Importantly, we validated our prediction of MybS2, TGA4, SPL12, AGL18, and DiV2 as regulators of seed lipid biosynthesis. We elucidated the molecular mechanism of MybS2 and show that it induces purple acid phosphatase family genes and lipid synthesis genes to enhance seed lipid content. This general approach has the potential to be extended to any species with sufficiently large gene expression datasets to find unique regulators of any trait-of-interest.

PMID: 38652750


J Hazard Mater , IF:10.588 , 2024 May , V469 : P134085 doi: 10.1016/j.jhazmat.2024.134085

Plant growth-promoting bacteria improve the Cd phytoremediation efficiency of soils contaminated with PE-Cd complex pollution by influencing the rhizosphere microbiome of sorghum.

Liu, Yong-Qi and Chen, Yan and Li, Yu-Ying and Ding, Chuan-Yu and Li, Bai-Lian and Han, Hui and Chen, Zhao-Jin

International Joint Laboratory of Watershed Ecological Security and Collaborative Innovation Center of Water Security for Water Source Region of Middle Route Project of South-North Water Diversion in Henan Province, School of Water Resource and Environmental Engineering, Nanyang Normal University, Nanyang 473061, China.; International Joint Laboratory of Watershed Ecological Security and Collaborative Innovation Center of Water Security for Water Source Region of Middle Route Project of South-North Water Diversion in Henan Province, School of Water Resource and Environmental Engineering, Nanyang Normal University, Nanyang 473061, China. Electronic address: 17657311626@163.com.; International Joint Laboratory of Watershed Ecological Security and Collaborative Innovation Center of Water Security for Water Source Region of Middle Route Project of South-North Water Diversion in Henan Province, School of Water Resource and Environmental Engineering, Nanyang Normal University, Nanyang 473061, China. Electronic address: zhaojin_chen@163.com.

Composite pollution by microplastics and heavy metals poses a potential threat to the soilplant system and has received increasing attention. Plant growth-promoting bacteria (PGPB) have good application potential for the remediation of combined microplastic and heavy metal pollution, but few related studies exist. The present study employed a pot experiment to investigate the effects of inoculation with the PGPB Bacillus sp. SL-413 and Enterobacter sp. VY-1 on sorghum growth and Cd accumulation under conditions of combined cadmium (Cd) and polyethylene (PE) pollution. Cd+PE composite contamination led to a significant reduction in sorghum length and biomass due to increased toxicity. Inoculation with Bacillus sp. SL-413 and Enterobacter sp. VY-1 alleviated the stress caused by Cd+PE complex pollution, and the dry weight of sorghum increased by 25.7% to 46.1% aboveground and by 12.3% to 45.3% belowground. Bacillus sp. SL-413 and Enterobacter sp. VY-1 inoculation increased the Cd content and accumulation in sorghum and improved the phytoremediation efficiency of Cd. The inoculation treatment effectively alleviated the nutrient stress caused by the reduction in soil mineral nutrients due to Cd+PE composite pollution. The composition of the soil bacterial communities was also affected by the Cd, Cd+PE and bacterial inoculation treatments, which affected the diversity of the soil bacterial communities. Network analyses indicated that bacterial inoculation regulated the interaction of rhizospheric microorganisms and increased the stability of soil bacterial communities. The Mantel test showed that the changes in the soil bacterial community and function due to inoculation with Bacillus sp. SL-413 and Enterobacter sp. VY-1 were important factors influencing sorghum growth and Cd remediation efficiency. The results of this study will provide new evidence for the research on joint plantmicrobe remediation of heavy metal and microplastic composite pollution.

PMID: 38522197


New Phytol , IF:10.151 , 2024 Jun , V242 (5) : P1911-1918 doi: 10.1111/nph.19734

Isotopically nonstationary metabolic flux analysis of plants: recent progress and future opportunities.

Koley, Somnath and Jyoti, Poonam and Lingwan, Maneesh and Allen, Doug K

Donald Danforth Plant Science Center, 975 North Warson Road, St Louis, MO, 63132, USA.; United States Department of Agriculture, Agriculture Research Service, 975 North Warson Road, St Louis, MO, 63132, USA.

Metabolic flux analysis (MFA) is a valuable tool for quantifying cellular phenotypes and to guide plant metabolic engineering. By introducing stable isotopic tracers and employing mathematical models, MFA can quantify the rates of metabolic reactions through biochemical pathways. Recent applications of isotopically nonstationary MFA (INST-MFA) to plants have elucidated nonintuitive metabolism in leaves under optimal and stress conditions, described coupled fluxes for fast-growing algae, and produced a synergistic multi-organ flux map that is a first in MFA for any biological system. These insights could not be elucidated through other approaches and show the potential of INST-MFA to correct an oversimplified understanding of plant metabolism.

PMID: 38628036


New Phytol , IF:10.151 , 2024 Jun , V242 (5) : P2059-2076 doi: 10.1111/nph.19737

Genome-wide association study and network analysis of in vitro transformation in Populus trichocarpa support key roles of diverse phytohormone pathways and cross talk.

Nagle, Michael F and Yuan, Jialin and Kaur, Damanpreet and Ma, Cathleen and Peremyslova, Ekaterina and Jiang, Yuan and Goralogia, Greg S and Magnuson, Anna and Li, Jia Yi and Muchero, Wellington and Fuxin, Li and Strauss, Steven H

Department of Forest Ecosystems & Society, Oregon State University, Corvallis, OR, 97331, USA.; School of Electrical Engineering and Computer Science, Oregon State University, Corvallis, OR, 97331, USA.; Statistics Department, Oregon State University, Corvallis, OR, 97331, USA.; Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN, 37830, USA.; Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, 37830, USA.; Bredesen Center for Interdisciplinary Research, University of Tennessee, Knoxville, TN, 37996, USA.

Wide variation in amenability to transformation and regeneration (TR) among many plant species and genotypes presents a challenge to the use of genetic engineering in research and breeding. To help understand the causes of this variation, we performed association mapping and network analysis using a population of 1204 wild trees of Populus trichocarpa (black cottonwood). To enable precise and high-throughput phenotyping of callus and shoot TR, we developed a computer vision system that cross-referenced complementary red, green, and blue (RGB) and fluorescent-hyperspectral images. We performed association mapping using single-marker and combined variant methods, followed by statistical tests for epistasis and integration of published multi-omic datasets to identify likely regulatory hubs. We report 409 candidate genes implicated by associations within 5 kb of coding sequences, and epistasis tests implicated 81 of these candidate genes as regulators of one another. Gene ontology terms related to protein-protein interactions and transcriptional regulation are overrepresented, among others. In addition to auxin and cytokinin pathways long established as critical to TR, our results highlight the importance of stress and wounding pathways. Potential regulatory hubs of signaling within and across these pathways include GROWTH REGULATORY FACTOR 1 (GRF1), PHOSPHATIDYLINOSITOL 4-KINASE beta1 (PI-4Kbeta1), and OBF-BINDING PROTEIN 1 (OBP1).

PMID: 38650352


New Phytol , IF:10.151 , 2024 May , V242 (3) : P1307-1323 doi: 10.1111/nph.19660

Genetic underpinnings of arthropod community distributions in Populus trichocarpa.

Simon, Sandra J and Furches, Anna and Chhetri, Hari and Evans, Luke and Abeyratne, Chanaka Roshan and Jones, Piet and Wimp, Gina and Macaya-Sanz, David and Jacobson, Daniel and Tschaplinski, Timothy J and Tuskan, Gerald A and DiFazio, Stephen P

Department of Biology, West Virginia University, Morgantown, WV, 26506, USA.; Biosciences Division and Center for Bioenergy Innovation, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.; The Bredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville, TN, 37996, USA.; Computational Systems Biology Group, Oak Ridge National Laboratory, Oak Ridge, TN, 37831, USA.; Institute for Behavioral Genetics, University of Colorado Boulder, Boulder, CO, 80309, USA.; Department of Biology, Georgetown University, Washington, DC, 20057, USA.

Community genetics seeks to understand the mechanisms by which natural genetic variation in heritable host phenotypes can encompass assemblages of organisms such as bacteria, fungi, and many animals including arthropods. Prior studies that focused on plant genotypes have been unable to identify genes controlling community composition, a necessary step to predict ecosystem structure and function as underlying genes shift within plant populations. We surveyed arthropods within an association population of Populus trichocarpa in three common gardens to discover plant genes that contributed to arthropod community composition. We analyzed our surveys with traditional single-trait genome-wide association analysis (GWAS), multitrait GWAS, and functional networks built from a diverse set of plant phenotypes. Plant genotype was influential in structuring arthropod community composition among several garden sites. Candidate genes important for higher level organization of arthropod communities had broadly applicable functions, such as terpenoid biosynthesis and production of dsRNA binding proteins and protein kinases, which may be capable of targeting multiple arthropod species. We have demonstrated the ability to detect, in an uncontrolled environment, individual genes that are associated with the community assemblage of arthropods on a host plant, further enhancing our understanding of genetic mechanisms that impact ecosystem structure.

PMID: 38488269


Metab Eng , IF:9.783 , 2024 May , V83 : P86-101 doi: 10.1016/j.ymben.2024.03.009

Resource allocation modeling for autonomous prediction of plant cell phenotypes.

Goelzer, Anne and Rajjou, Loic and Chardon, Fabien and Loudet, Olivier and Fromion, Vincent

Universite Paris-Saclay, INRAE, MaIAGE, 78350, Jouy-en-Josas, France. Electronic address: anne.goelzer@inrae.fr.; Universite Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France.; Universite Paris-Saclay, INRAE, MaIAGE, 78350, Jouy-en-Josas, France. Electronic address: vincent.fromion@inrae.fr.

Predicting the plant cell response in complex environmental conditions is a challenge in plant biology. Here we developed a resource allocation model of cellular and molecular scale for the leaf photosynthetic cell of Arabidopsis thaliana, based on the Resource Balance Analysis (RBA) constraint-based modeling framework. The RBA model contains the metabolic network and the major macromolecular processes involved in the plant cell growth and survival and localized in cellular compartments. We simulated the model for varying environmental conditions of temperature, irradiance, partial pressure of CO(2) and O(2), and compared RBA predictions to known resource distributions and quantitative phenotypic traits such as the relative growth rate, the C:N ratio, and finally to the empirical characteristics of CO(2) fixation given by the well-established Farquhar model. In comparison to other standard constraint-based modeling methods like Flux Balance Analysis, the RBA model makes accurate quantitative predictions without the need for empirical constraints. Altogether, we show that RBA significantly improves the autonomous prediction of plant cell phenotypes in complex environmental conditions, and provides mechanistic links between the genotype and the phenotype of the plant cell.

PMID: 38561149


Crit Rev Biotechnol , IF:8.429 , 2024 May : P1-17 doi: 10.1080/07388551.2024.2336529

Chromatin modifications and memory in regulation of stress-related polyphenols: finding new ways to control flavonoid biosynthesis.

Bulgakov, Victor P

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia.

The influence of epigenetic factors on plant defense responses and the balance between growth and defense is becoming a central area in plant biology. It is believed that the biosynthesis of secondary metabolites can be regulated by epigenetic factors, but this is not associated with the formation of a "memory" to the previous biosynthetic status. This review shows that some epigenetic effects can result in epigenetic memory, which opens up new areas of research in secondary metabolites, in particular flavonoids. Plant-controlled chromatin modifications can lead to the generation of stress memory, a phenomenon through which information regarding past stress cues is retained, resulting in a modified response to recurring stress. How deeply are the mechanisms of chromatin modification and memory generation involved in the control of flavonoid biosynthesis? This article collects available information from the literature and interactome databases to address this issue. Visualization of the interaction of chromatin-modifying proteins with the flavonoid biosynthetic machinery is presented. Chromatin modifiers and "bookmarks" that may be involved in the regulation of flavonoid biosynthesis through memory have been identified. Through different mechanisms of chromatin modification, plants can harmonize flavonoid metabolism with: stress responses, developmental programs, light-dependent processes, flowering, and longevity programs. The available information points to the possibility of developing chromatin-modifying technologies to control flavonoid biosynthesis.

PMID: 38697923


Plant Physiol , IF:8.34 , 2024 May doi: 10.1093/plphys/kiae273

Transcriptional Landscape and Dynamics Involved in Sugar and Acid Accumulation during Apple Fruit Development.

Li, Baiyun and Zhu, Lingcheng and Yang, Nanxiang and Qu, Shengtao and Cao, Wenjing and Ma, Wenfang and Wei, Xiaoyu and Ma, Baiquan and Ma, Fengwang and Fu, Aigen and Li, Mingjun

State Key Laboratory for Crop Stress Resistance and High-Efficiency Production/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling, Shaanxi, 712100, China.; Chinese Education Ministry's Key Laboratory of Western Resources and Modern Biotechnology, Key Laboratory of Biotechnology Shaanxi Province, College of Life Sciences, Northwest University, Xi'an, Shaanxi, 710069, China.

In fleshy fruit, sugars and acids are central components of fruit flavor and quality. To date, the mechanisms underlying transcriptional regulation of sugar and acid during fruit development remain largely unknown. Here, we combined ATAC-seq with RNA-seq to investigate the genome-wide chromatin accessibility and to identify putative transcription factors related to sugar and acid accumulation during apple (Malus domestica) fruit development. By integrating the differentially accessible regions (DARs) and differentially expressed genes (DEGs), we generated a global dataset of promoter-accessibility- and expression-increased genes (PEIGs). Using this strategy, we constructed a transcriptional regulatory network enabling screening for key transcription factors and target genes involved in sugar and acid accumulation. Among these transcription factors, five fruit-specific Dof (DNA binding with one finger) genes were selected to confirm their regulatory effects, and our results showed that they could affect sugar or acid concentration by regulating the expression of sugar or acid metabolism-related genes in apple fruits. Our transcriptional regulatory network provides a suitable platform to identify candidate genes that control sugar and acid accumulation. Meanwhile, our dataset will aid in analyzing other characteristics of apple fruit that have not been illuminated previously. Overall, these findings support a better understanding of the regulatory dynamics during apple fruit development and lay a foundation for quality improvement of apple.

PMID: 38728429


Sci Total Environ , IF:7.963 , 2024 May , V935 : P173413 doi: 10.1016/j.scitotenv.2024.173413

Response patterns of the microbiome during hexavalent chromium remediation by Tagetes erecta L.

Xiao, Juanjuan and Wang, Deying and Sinchan, Banerjee and Mushinski, Ryan and Jin, Decai and Deng, Ye

Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China.; School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK.; Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China; College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: dcjin@rcees.ac.cn.

Chromium pollution, particularly hexavalent chromium [Cr(VI)], may threaten the environment and human health. This study investigated the potential of Tagetes erecta L. (Aztec marigold) for phytoremediation of soil contaminated with Cr(VI), and focused on the effects of varying concentrations of Cr(VI) on both the physicochemical properties of soil and microbiome of Tagetes erecta L. We observed that Tagetes erecta L. showed tolerance to Cr(VI) stress and maintained normal growth under these conditions, as indicated by bioconcentration factors of 0.33-0.53 in shoots and 0.39-0.70 in roots. Meanwhile, the structure and diversity of bacterial communities were significantly affected by Cr(VI) pollution. Specifically, Cr(VI) had a more significant effect on the microbial community structure in the endophytic of Tagetes erecta L. than in the rhizosphere (p < 0.05). The genera Devosia and Methylobacillus were positively correlated with Cr(VI) concentrations. Biomarkers such as Bacilli and Pseudonocardia were identified under the different Cr(VI)-contaminated treatments using LEfSe. In addition, the interaction and stability of the endophytic microbiome were enhanced under Cr(VI) stress. This study explored the interactions between heavy metals, microorganisms, and plants, providing valuable insights for developing in situ bioremediation of Cr(VI)-contaminated soils.

PMID: 38788956


Sci Total Environ , IF:7.963 , 2024 Jun , V927 : P171301 doi: 10.1016/j.scitotenv.2024.171301

Impact of harmful algal bloom severity on bacterial communities in a full-scale biological filtration system for drinking water treatment.

Jeon, Youchul and Li, Lei and Bhatia, Mudit and Ryu, Hodon and Santo Domingo, Jorge W and Brown, Jess and Goetz, Jake and Seo, Youngwoo

Department of Civil and Environmental Engineering, University of Toledo, Mail Stop 307, 3006 Nitschke Hall, Toledo, OH 43606, United States of America.; Water Infrastructure Division, Center for Environmental Solutions and Emergency Response, U.S. Environmental Protection Agency, Cincinnati, OH 45268, United States of America.; Carollo Engineers' Research and Development Practice, Costa Mesa, CA 92626, United States of America.; City of Toledo Colins Park Water Treatment, Toledo, OH 43605, United States of America.; Department of Civil and Environmental Engineering, University of Toledo, Mail Stop 307, 3006 Nitschke Hall, Toledo, OH 43606, United States of America; Department of Chemical and Engineering, University of Toledo, Mail Stop 307, 3048 Nitschke Hall, Toledo, OH 43606, United States of America. Electronic address: Youngwoo.Seo@utoledo.edu.

The occurrence of harmful algal blooms (HABs) in freshwater environments has been expanded worldwide with growing frequency and severity. HABs can pose a threat to public water supplies, raising concerns about safety of treated water. Many studies have provided valuable information about the impacts of HABs and management strategies on the early-stage treatment processes (e.g., pre-oxidation and coagulation/flocculation) in conventional drinking water treatment plants (DWTPs). However, the potential effect of HAB-impacted water in the granular media filtration has not been well studied. Biologically-active filters (BAFs), which are used in drinking water treatment and rely largely on bacterial community interactions, have not been examined during HABs in full-scale DWTPs. In this study, we assessed the bacterial community structure of BAFs, functional profiles, assembly processes, and bio-interactions in the community during both severe and mild HABs. Our findings indicate that bacterial diversity in BAFs significantly decreases during severe HABs due to the predominance of bloom-associated bacteria (e.g., Spingopyxis, Porphyrobacter, and Sphingomonas). The excitation-emission matrix combined with parallel factor analysis (EEM-PARAFAC) confirmed that filter influent affected by the severe HAB contained a higher portion of protein-like substances than filter influent samples during a mild bloom. In addition, BAF community functions showed increases in metabolisms associated with intracellular algal organic matter (AOM), such as lipids and amino acids, during severe HABs. Further ecological process and network analyses revealed that severe HAB, accompanied by the abundance of bloom-associated taxa and increased nutrient availability, led to not only strong stochastic processes in the assembly process, but also a bacterial community with lower complexity in BAFs. Overall, this study provides deeper insights into BAF bacterial community structure, function, and assembly in response to HABs.

PMID: 38423320


Sci Total Environ , IF:7.963 , 2024 May , V937 : P173422 doi: 10.1016/j.scitotenv.2024.173422

The ethylene response factor gene, ThDRE1A, is involved in abscisic acid- and ethylene-mediated cadmium accumulation in Tamarix hispida.

Xie, Qingjun and Wang, Danni and Ding, Yuting and Gao, Wenshuo and Li, Jinghang and Cao, Chuanwang and Sun, Lili and Liu, Zhongyuan and Gao, Caiqiu

State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China; Key Laboratory of Sustainable Forest Ecosystem Management-Ministry of Education, Northeast Forestry University, Harbin 150040, China.; State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China.; Key Laboratory of Sustainable Forest Ecosystem Management-Ministry of Education, Northeast Forestry University, Harbin 150040, China.; State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin 150040, China. Electronic address: gaocaiqiu@nefu.edu.cn.

Tamarix hispida is highly tolerant to salt, drought and heavy metal stress and is a potential material for the remediation of cadmium (Cd)-contaminated soil under harsh conditions. In this study, T. hispida growth and chlorophyll content decreased, whereas flavonoid and carotenoid contents increased under long-term Cd stress (25 d). The aboveground components of T. hispida were collected for RNA-seq to investigate the mechanism of Cd accumulation. GO and KEGG enrichment analyses revealed that the differentially expressed genes (DEGs) were significantly enriched in plant hormone-related pathways. Exogenous hormone treatment and determination of Cd(2+) levels showed that ethylene (ETH) and abscisic acid (ABA) antagonists regulate Cd accumulation in T. hispida. Twenty-five transcription factors were identified as upstream regulators of hormone-related pathways. ThDRE1A, which was previously identified as an important regulatory factor, was selected for further analysis. The results indicated that ThABAH2.5 and ThACCO3.1 were direct target genes of ThDRE1A. The determination of Cd(2+), ABA, and ETH levels indicated that ThDRE1A plays an important role in Cd accumulation through the antagonistic regulation of ABA and ETH. In conclusion, these results reveal the molecular mechanism underlying Cd accumulation in plants and identify candidate genes for further research.

PMID: 38796019


mBio , IF:7.867 , 2024 May : Pe0350423 doi: 10.1128/mbio.03504-23

A transcription factor-mediated regulatory network controls fungal pathogen colonization of insect body cavities.

Deng, Juan and Huang, Shuaishuai and Kan, Yanze and Song, Yue and Zhao, Xin and Li, Ning and Yao, Xuewen and Luo, Zhibing and Zhang, Yongjun

Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), College of Plant Protection, Southwest University, Chongqing, China.; Key Laboratory of Entomology and Pest Control Engineering, Academy of Agricultural Sciences, Southwest University, Chongqing, China.; Beibei Culture Collection of Chongqing Agricultural Microbiology, Southwest University, Chongqing, China.; Ministry of Education Key Laboratory of Biodiversity and Eco-Environmental Protection of the Qinghai-Tibetan Plateau, School of Ecology and Environment, Tibet University, Tibet, China.

Successful host tissue colonization is crucial for fungal pathogens to cause mycosis and complete the infection cycle, in which fungal cells undergo a series of morphological transition-included cellular events to combat with hosts. However, many transcription factors (TFs) and their mediated networks regulating fungal pathogen colonization of host tissue are not well characterized. Here, a TF (BbHCR1)-mediated regulatory network was identified in an insect pathogenic fungus, Beauveria bassiana, that controlled insect hemocoel colonization. BbHCR1 was highly expressed in fungal cells after reaching insect hemocoel and controlled the yeast (in vivo blastospores)-to-hyphal morphological switch, evasion of immune defense response, and fungal virulence. Comparative analysis of RNA sequencing and chromatin immunoprecipitation sequencing identified a core set of BbHCR1 target genes during hemocoel colonization, in which abaA and brlA were targeted to limit the rapid switch from blastospores to hyphae and fungal virulence. Two targets encoding hypothetical proteins, HP1 and HP2, were activated and repressed by BbHCR1, respectively, which acted as a virulence factor and repressor, respectively, suggesting that BbHCR1 activated virulence factors but repressed virulence repressors during the colonization of insect hemocoel. BbHCR1 tuned the expression of two dominant hemocoel colonization-involved metabolite biosynthetic gene clusters, which linked its regulatory role in evasion of immune response. Those functions of BbHCR1 were found to be collaboratively regulated by Fus3- and Hog1-MAP kinases via phosphorylation. These findings have drawn a regulatory network in which Fus3- and Hog1-MAP kinases phosphorylate BbHCR1, which in turn controls the colonization of insect body cavities by regulating fungal morphological transition and virulence-implicated genes.IMPORTANCEFungal pathogens adopt a series of tactics for successful colonization in host tissues, which include morphological transition and the generation of toxic and immunosuppressive molecules. However, many transcription factors (TFs) and their linked pathways that regulate tissue colonization are not well characterized. Here, we identified a TF (BbHCR1)-mediated regulatory network that controls the insect fungal pathogen, Beauveria bassiana, colonization of insect hemocoel. During these processes, BbHCR1 targeted the fungal central development pathway for the control of yeast (blastospores)-to-hyphae morphological transition, activated virulence factors, and repressed virulence repressors by tuning the expression of two dominant hemocoel colonization-involved immunosuppressive and immunostimulatory metabolite biosynthetic gene clusters. The BbHCR1 regulatory function was governed by Fus3- and Hog1-MAP kinases. These findings led to a new regulatory network composed of Fus3- and Hog1-MAP kinases and BbHCR1 that control insect body cavity colonization by regulating fungal morphological transition and virulence-implicated genes.

PMID: 38747587


Plant Cell Environ , IF:7.228 , 2024 May doi: 10.1111/pce.14950

Regulatory networks of senescence-associated gene-transcription factors promote degradation in Moso bamboo shoots.

Zhang, Wenyu and Shi, Man and Yang, Kebin and Zhang, Junbo and Gao, Zhimin and El-Kassaby, Yousry A and Li, Quan and Cao, Tingting and Deng, Shixin and Qing, Hongsheng and Wang, Zhikang and Song, Xinzhang

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Hangzhou, China.; College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao, China.; International Center for Bamboo and Rattan, Beijing, China.; Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, British Columbia, Canada.

Bamboo cultivation, particularly Moso bamboo (Phyllostachys edulis), holds significant economic importance in various regions worldwide. Bamboo shoot degradation (BSD) severely affects productivity and economic viability. However, despite its agricultural consequences, the molecular mechanisms underlying BSD remain unclear. Consequently, we explored the dynamic changes of BSD through anatomy, physiology and the transcriptome. Our findings reveal ruptured protoxylem cells, reduced cell wall thickness and the accumulation of sucrose and reactive oxygen species (ROS) during BSD. Transcriptomic analysis underscored the importance of genes related to plant hormone signal transduction, sugar metabolism and ROS homoeostasis in this process. Furthermore, BSD appears to be driven by the coexpression regulatory network of senescence-associated gene transcription factors (SAG-TFs), specifically PeSAG39, PeWRKY22 and PeWRKY75, primarily located in the protoxylem of vascular bundles. Yeast one-hybrid and dual-luciferase assays demonstrated that PeWRKY22 and PeWRKY75 activate PeSAG39 expression by binding to its promoter. This study advanced our understanding of the molecular regulatory mechanisms governing BSD, offering a valuable reference for enhancing Moso bamboo forest productivity.

PMID: 38752443


J Exp Bot , IF:6.992 , 2024 May , V75 (10) : P2781-2798 doi: 10.1093/jxb/erae051

Gene regulatory networks underlying sulfate deficiency responses in plants.

Fernandez, Jose David and Mino, Ignacio and Canales, Javier and Vidal, Elena A

Centro de Genomica y Bioinformatica, Facultad de Ciencias, Ingenieria y Tecnologia, Universidad Mayor, 8580745, Santiago, Chile.; Agencia Nacional de Investigacion y Desarrollo - Millennium Science Initiative Program, Millennium Institute for Integrative Biology, 7500565, Santiago, Chile.; Programa de Doctorado en Genomica Integrativa, Vicerrectoria de Investigacion, Universidad Mayor, 8580745, Santiago, Chile.; Instituto de Bioquimica y Microbiologia, Facultad de Ciencias, Universidad Austral de Chile, 5110566, Valdivia, Chile.; Escuela de Biotecnologia, Facultad de Ciencias, Ingenieria y Tecnologia, Universidad Mayor, 8580745, Santiago, Chile.

Sulfur (S) is an essential macronutrient for plants and its availability in soils is an important determinant for growth and development. Current regulatory policies aimed at reducing industrial S emissions together with changes in agronomical practices have led to a decline in S contents in soils worldwide. Deficiency of sulfate-the primary form of S accessible to plants in soil-has adverse effects on both crop yield and nutritional quality. Hence, recent research has increasingly focused on unraveling the molecular mechanisms through which plants detect and adapt to a limiting supply of sulfate. A significant part of these studies involves the use of omics technologies and has generated comprehensive catalogs of sulfate deficiency-responsive genes and processes, principally in Arabidopsis together with a few studies centering on crop species such as wheat, rice, or members of the Brassica genus. Although we know that sulfate deficiency elicits an important reprogramming of the transcriptome, the transcriptional regulators orchestrating this response are not yet well understood. In this review, we summarize our current knowledge of gene expression responses to sulfate deficiency and recent efforts towards the identification of the transcription factors that are involved in controlling these responses. We further compare the transcriptional response and putative regulators between Arabidopsis and two important crop species, rice and tomato, to gain insights into common mechanisms of the response to sulfate deficiency.

PMID: 38366662


Food Res Int , IF:6.475 , 2024 Jul , V187 : P114359 doi: 10.1016/j.foodres.2024.114359

Characterization of the aroma-active compounds in Xiaokeng green tea by three pretreatment methods combined with gas chromatography-olfactometry (GC-O).

Gan, Shiya and Chen, Yingqi and Zhao, Lei and Zhao, Xiaoyi and Qiu, Tong and Zhai, Xiaoting and Dai, Qianying

State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei 230036, People's Republic of China; Key Laboratory of Tea Biology and Tea Processing of Ministry of Agriculture and Rural Affairs, Hefei 230036, People's Republic of China; International Joint Laboratory on Tea Chemistry and Health Effects of Ministry of Education, Anhui Agricultural University, Hefei 230036, People's Republic of China.; State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei 230036, People's Republic of China; Key Laboratory of Tea Biology and Tea Processing of Ministry of Agriculture and Rural Affairs, Hefei 230036, People's Republic of China; International Joint Laboratory on Tea Chemistry and Health Effects of Ministry of Education, Anhui Agricultural University, Hefei 230036, People's Republic of China. Electronic address: xiaotingzhai@ahau.edu.cn.; State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei 230036, People's Republic of China; Key Laboratory of Tea Biology and Tea Processing of Ministry of Agriculture and Rural Affairs, Hefei 230036, People's Republic of China; International Joint Laboratory on Tea Chemistry and Health Effects of Ministry of Education, Anhui Agricultural University, Hefei 230036, People's Republic of China. Electronic address: daiqianying@ahau.edu.cn.

Chinese Xiaokeng green tea (XKGT) possesses elegant and fascinating aroma characteristics, but its key odorants are still unknown. In this study, 124 volatile compounds in the XKGT infusion were identified by headspace-solid phase microextraction (HS-SPME), stir bar sorptive extraction (SBSE), and solvent extraction-solid phase extraction (SE-SPE) combined with gas chromatography-mass spectrometry (GC-MS). Comparing these three pretreatments, we found HS-SPME was more efficient for headspace compounds while SE-SPE was more efficient for volatiles with higher boiling points. Furthermore, SBSE showed more sensitive to capture ketones then was effective to the application of pretreatment of aroma analysis in green tea. The aroma intensities (AIs) were further identified by gas chromatography-olfactometry (GC-O). According to the AI and relative odor activity value (rOAV), 27 compounds were identified as aroma-active compounds. Quantitative descriptive analysis (QDA) showed that the characteristic aroma attributes of XKGT were chestnut-like, corn-like, fresh, and so on. The results of network analysis showed that (E, Z)-2,6-nonadienal, nonanal, octanal and nerolidol were responsible for the fresh aroma. Similarly, dimethyl sulfide, (E, E)-2,4-heptadienal, (E)-2-octenal and beta-cyclocitral contributed to the corn-like aroma. Furthermore, indole was responsible for the chestnut-like and soybean-like aroma. This study contributes to a better understanding of the molecular mechanism of the aroma characteristics of XKGT.

PMID: 38763643


Plant J , IF:6.417 , 2024 Jun , V118 (5) : P1668-1688 doi: 10.1111/tpj.16690

Cell-type-specific transcriptomics uncovers spatial regulatory networks in bioenergy sorghum stems.

Fu, Jie and McKinley, Brian and James, Brandon and Chrisler, William and Markillie, Lye Meng and Gaffrey, Matthew J and Mitchell, Hugh D and Riaz, Muhammad Rizwan and Marcial, Brenda and Orr, Galya and Swaminathan, Kankshita and Mullet, John and Marshall-Colon, Amy

Department of Plant Biology, University of Illinois Urbana-Champaign, Urbana, Illinois, 61801, USA.; DOE Center for Advanced Bioenergy and Bioproducts Innovation, Urbana, Illinois, 61801, USA.; Department of Biochemistry and Biophysics, Texas A&M University, College Station, Texas, 77843, USA.; DOE Great Lakes Bioenergy Resource Center, Madison, Wisconsin, 53726, USA.; HudsonAlpha Institute for Biotechnology, Huntsville, Alabama, 35806, USA.; Pacific Northwest National Laboratory, Richland, Washington, 99354, USA.

Bioenergy sorghum is a low-input, drought-resilient, deep-rooting annual crop that has high biomass yield potential enabling the sustainable production of biofuels, biopower, and bioproducts. Bioenergy sorghum's 4-5 m stems account for ~80% of the harvested biomass. Stems accumulate high levels of sucrose that could be used to synthesize bioethanol and useful biopolymers if information about cell-type gene expression and regulation in stems was available to enable engineering. To obtain this information, laser capture microdissection was used to isolate and collect transcriptome profiles from five major cell types that are present in stems of the sweet sorghum Wray. Transcriptome analysis identified genes with cell-type-specific and cell-preferred expression patterns that reflect the distinct metabolic, transport, and regulatory functions of each cell type. Analysis of cell-type-specific gene regulatory networks (GRNs) revealed that unique transcription factor families contribute to distinct regulatory landscapes, where regulation is organized through various modes and identifiable network motifs. Cell-specific transcriptome data was combined with known secondary cell wall (SCW) networks to identify the GRNs that differentially activate SCW formation in vascular sclerenchyma and epidermal cells. The spatial transcriptomic dataset provides a valuable source of information about the function of different sorghum cell types and GRNs that will enable the engineering of bioenergy sorghum stems, and an interactive web application developed during this project will allow easy access and exploration of the data (https://mc-lab.shinyapps.io/lcm-dataset/).

PMID: 38407828


Int J Mol Sci , IF:5.923 , 2024 May , V25 (10) doi: 10.3390/ijms25105501

Transcriptome Analysis of Sesame (Sesamum indicum L.) Reveals the LncRNA and mRNA Regulatory Network Responding to Low Nitrogen Stress.

Zhang, Pengyu and Li, Feng and Tian, Yuan and Wang, Dongyong and Fu, Jinzhou and Rong, Yasi and Wu, Yin and Gao, Tongmei and Zhang, Haiyang

Henan Sesame Research Center, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China.; The Shennong Laboratory, Zhengzhou 450002, China.

Nitrogen is one of the important factors restricting the development of sesame planting and industry in China. Cultivating sesame varieties tolerant to low nitrogen is an effective way to solve the problem of crop nitrogen deficiency. To date, the mechanism of low nitrogen tolerance in sesame has not been elucidated at the transcriptional level. In this study, two sesame varieties Zhengzhi HL05 (ZZ, nitrogen efficient) and Burmese prolific (MD, nitrogen inefficient) in low nitrogen were used for RNA-sequencing. A total of 3964 DEGs (differentially expressed genes) and 221 DELs (differentially expressed lncRNAs) were identified in two sesame varieties at 3d and 9d after low nitrogen stress. Among them, 1227 genes related to low nitrogen tolerance are mainly located in amino acid metabolism, starch and sucrose metabolism and secondary metabolism, and participate in the process of transporter activity and antioxidant activity. In addition, a total of 209 pairs of lncRNA-mRNA were detected, including 21 pairs of trans and 188 cis. WGCNA (weighted gene co-expression network analysis) analysis divided the obtained genes into 29 modules; phenotypic association analysis identified three low-nitrogen response modules; through lncRNA-mRNA co-expression network, a number of hub genes and cis/trans-regulatory factors were identified in response to low-nitrogen stress including GS1-2 (glutamine synthetase 1-2), PAL (phenylalanine ammonia-lyase), CHS (chalcone synthase, CHS), CAB21 (chlorophyll a-b binding protein 21) and transcription factors MYB54, MYB88 and NAC75 and so on. As a trans regulator, lncRNA MSTRG.13854.1 affects the expression of some genes related to low nitrogen response by regulating the expression of MYB54, thus responding to low nitrogen stress. Our research is the first to provide a more comprehensive understanding of DEGs involved in the low nitrogen stress of sesame at the transcriptome level. These results may reveal insights into the molecular mechanisms of low nitrogen tolerance in sesame and provide diverse genetic resources involved in low nitrogen tolerance research.

PMID: 38791539


Front Pharmacol , IF:5.81 , 2024 , V15 : P1357381 doi: 10.3389/fphar.2024.1357381

Utilizing metabolomics and network analysis to explore the effects of artificial production methods on the chemical composition and activity of agarwood.

Hou, Wencheng and Feng, Jian and Sun, Yuanyuan and Chen, Xiqin and Liu, Yangyang and Wei, Jianhe

Hainan Provincial Key Laboratory of Resources Conservation and Development of Southern Medicine and Key Laboratory of State Administration of Traditional Chinese Medicine for Agarwood Sustainable Utilization, Hainan Branch of the Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Haikou, China.; Key Laboratory of Bioactive Substances and Resources Utilization of Chinese Herbal Medicine, Ministry of Education and National Engineering Laboratory for Breeding of Endangered Medicinal Materials, Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China.

Introduction: Agarwood is a traditional aromatic southern medicine. It has a long history of being used in traditional Chinese aromatherapy to treat insomnia, anxiety and depression. Due to the scarcity of wild resources, people have planted trees successfully and begun to explore various agarwood-inducing techniques. This study comparative analysis of volatile metabolites in agarwood produced by various inducing techniques and its potential sleep-promoting, anti-anxiety and anti-depressant network pharmacological activities. Methods: A total of 23 batches of two types of agarwood were collected, one of which was produced by artificial techniques, including 6 batches of TongTi (TT) agarwood produced by "Agar-Wit" and 6 batches of HuoLao (HL) agarwood produced by "burning, chisel and drilling", while the other was collected from the wild, including 6 batches of BanTou (BT) agarwood with trunks broken due to natural or man-made factors and 5 batches of ChongLou (CL) agarwood with trunks damaged by moth worms. The study employed metabolomics combined with network analysis to compare the differences in volatile metabolites of agarwood produced by four commonly used inducing techniques, and explored their potential roles and possible action targets in promoting sleep, reducing anxiety, and alleviating depression. Results: A total of 147 volatile metabolites were detected in agarwood samples, mainly including small aromatic hydrocarbons, sesquiterpenes and 2-(2-phenylethyl) chromone and their pyrolysis products. The results showed composition of metabolites was minimally influenced by the agarwood induction method. However, their concentrations exhibited significant variations, with 17 metabolites showing major differences. The two most distinct metabolites were 6-methoxy-2-(2-phenylethyl) chromone and 6,7-dimethoxy-2-(2-phenylethyl) chromone. Among the volatile metabolites, 142 showed promising potential in treating insomnia, anxiety, and depression, implicating various biological and signaling pathways, predominantly ALB and TNF targets. The top three active metabolites identified were 2-(2-phenylethyl) chromone, 1,5-diphenylpent-1-en-3-one, and 6-methoxy-2-[2-(4'-methoxyphenyl) ethyl] chromone, with their relative content in the four types of agarwood being TT>HL>CL>BT. Conclusion: The differences in the content of 2-(2-phenylethyl) chromones suggest that they may be responsible for the varying therapeutic activities observed in different types of agarwood aromatherapy. This study offers theoretical support for the selection of agarwood in aromatherapy practices.

PMID: 38774207


Front Plant Sci , IF:5.753 , 2024 , V15 : P1403060 doi: 10.3389/fpls.2024.1403060

Regulatory microRNAs and phasiRNAs of paclitaxel biosynthesis in Taxus chinensis.

Sun, Ming-Sheng and Jia, Yan and Chen, Xin-Yi and Chen, Ji-Shi and Guo, Ying and Fu, Fang-Fang and Xue, Liang-Jiao

State Key Laboratory of Tree Genetics and Breeding, Co-Innovation Center for Sustainable Forestry in Southern China, Key Laboratory of Tree Genetics and Biotechnology of Educational Department of China, Nanjing Forestry University, Nanjing, China.

Paclitaxel (trade name Taxol) is a rare diterpenoid with anticancer activity isolated from Taxus. At present, paclitaxel is mainly produced by the semi-synthetic method using extract of Taxus tissues as raw materials. The studies of regulatory mechanisms in paclitaxel biosynthesis would promote the production of paclitaxel through tissue/cell culture approaches. Here, we systematically identified 990 transcription factors (TFs), 460 microRNAs (miRNAs), and 160 phased small interfering RNAs (phasiRNAs) in Taxus chinensis to explore their interactions and potential roles in regulation of paclitaxel synthesis. The expression levels of enzyme genes in cone and root were higher than those in leaf and bark. Nearly all enzyme genes in the paclitaxel synthesis pathway were significantly up-regulated after jasmonate treatment, except for GGPPS and CoA Ligase. The expression level of enzyme genes located in the latter steps of the synthesis pathway was significantly higher in female barks than in male. Regulatory TFs were inferred through co-expression network analysis, resulting in the identification of TFs from diverse families including MYB and AP2. Genes with ADP binding and copper ion binding functions were overrepresented in targets of miRNA genes. The miRNA targets were mainly enriched with genes in plant hormone signal transduction, mRNA surveillance pathway, cell cycle and DNA replication. Genes in oxidoreductase activity, protein-disulfide reductase activity were enriched in targets of phasiRNAs. Regulatory networks were further constructed including components of enzyme genes, TFs, miRNAs, and phasiRNAs. The hierarchical regulation of paclitaxel production by miRNAs and phasiRNAs indicates a robust regulation at post-transcriptional level. Our study on transcriptional and posttranscriptional regulation of paclitaxel synthesis provides clues for enhancing paclitaxel production using synthetic biology technology.

PMID: 38779066


Plant Physiol Biochem , IF:4.27 , 2024 May , V210 : P108609 doi: 10.1016/j.plaphy.2024.108609

Integrated omics approach reveals the molecular pathways activated in tomato by Kocuria rhizophila, a soil plant growth-promoting bacterium.

Mauceri, Antonio and Puccio, Guglielmo and Faddetta, Teresa and Abbate, Loredana and Polito, Giulia and Caldiero, Ciro and Renzone, Giovanni and Lo Pinto, Margot and Alibrandi, Pasquale and Vaccaro, Edoardo and Abenavoli, Maria Rosa and Scaloni, Andrea and Sunseri, Francesco and Cavalieri, Vincenzo and Palumbo Piccionello, Antonio and Gallo, Giuseppe and Mercati, Francesco

University Mediterranea of Reggio Calabria, AGRARIA Department, Localita Feo di Vito, 89122, Reggio Calabria, Italy.; National Research Council, Institute of Biosciences and Bioresources (IBBR), Via Ugo La Malfa 153, 90146, Palermo, Italy; University of Palermo, SAAF Department, Viale Delle Scienze, 90128, Palermo, Italy.; University of Palermo, STEBICEF Department, Viale Delle Scienze, 90128, Palermo, Italy.; National Research Council, Institute of Biosciences and Bioresources (IBBR), Via Ugo La Malfa 153, 90146, Palermo, Italy.; National Research Council, Proteomics, Metabolomics and Mass Spectrometry Laboratory (ISPAAM), Piazzale E. Fermi 1, 80055, Portici, (Napoli), Italy.; Mugavero Teresa S.A.S., Corso Umberto e Margherita 1B, 90018, Termini Imerese, (Palermo), Italy.; University of Palermo, STEBICEF Department, Viale Delle Scienze, 90128, Palermo, Italy; NBFC, National Biodiversity Future Center, Piazza Marina 61, 90133, Palermo, Italy.; National Research Council, Institute of Biosciences and Bioresources (IBBR), Via Ugo La Malfa 153, 90146, Palermo, Italy. Electronic address: francesco.mercati@cnr.it.

Plant microbial biostimulants application has become a promising and eco-friendly agricultural strategy to improve crop yields, reducing chemical inputs for more sustainable cropping systems. The soil dwelling bacterium Kocuria rhizophila was previously characterized as Plant Growth Promoting Bacteria (PGPB) for its multiple PGP traits, such as indole-3-acetic acid production, phosphate solubilization capability and salt and drought stress tolerance. Here, we evaluated by a multi-omics approach, the PGP activity of K. rhizophila on tomato, revealing the molecular pathways by which it promotes plant growth. Transcriptomic analysis showed several up-regulated genes mainly related to amino acid metabolism, cell wall organization, lipid and secondary metabolism, together with a modulation in the DNA methylation profile, after PGPB inoculation. In agreement, proteins involved in photosynthesis, cell division, and plant growth were highly accumulated by K. rhizophila. Furthermore, "amino acid and peptides", "monosaccharides", and "TCA" classes of metabolites resulted the most affected by PGPB treatment, as well as dopamine, a catecholamine neurotransmitter mediating plant growth through S-adenosylmethionine decarboxylase (SAMDC), a gene enhancing the vegetative growth, up-regulated in tomato by K. rhizophila treatment. Interestingly, eight gene modules well correlated with differentially accumulated proteins (DAPs) and metabolites (DAMs), among which two modules showed the highest correlation with nine proteins, including a nucleoside diphosphate kinase, and cytosolic ascorbate peroxidase, as well as with several amino acids and metabolites involved in TCA cycle. Overall, our findings highlighted that sugars and amino acids, energy regulators, involved in tomato plant growth, were strongly modulated by the K. rhizophila-plant interaction.

PMID: 38615442


BMC Plant Biol , IF:4.215 , 2024 May , V24 (1) : P373 doi: 10.1186/s12870-024-05086-5

A method for mining condition-specific co-expressed genes in Camellia sinensis based on k-means clustering.

Zheng, Xinghai and Lim, Peng Ken and Mutwil, Marek and Wang, Yuefei

Tea Research Institute, Zhejiang University, Hangzhou, 310058, Zhejiang, China. xhzheng@zju.edu.cn.; School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore, 637551, Singapore. xhzheng@zju.edu.cn.; School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore, 637551, Singapore.; School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore, 637551, Singapore. mutwil@ntu.edu.sg.; Tea Research Institute, Zhejiang University, Hangzhou, 310058, Zhejiang, China. zdcy@zju.edu.cn.

BACKGROUND: As one of the world's most important beverage crops, tea plants (Camellia sinensis) are renowned for their unique flavors and numerous beneficial secondary metabolites, attracting researchers to investigate the formation of tea quality. With the increasing availability of transcriptome data on tea plants in public databases, conducting large-scale co-expression analyses has become feasible to meet the demand for functional characterization of tea plant genes. However, as the multidimensional noise increases, larger-scale co-expression analyses are not always effective. Analyzing a subset of samples generated by effectively downsampling and reorganizing the global sample set often leads to more accurate results in co-expression analysis. Meanwhile, global-based co-expression analyses are more likely to overlook condition-specific gene interactions, which may be more important and worthy of exploration and research. RESULTS: Here, we employed the k-means clustering method to organize and classify the global samples of tea plants, resulting in clustered samples. Metadata annotations were then performed on these clustered samples to determine the "conditions" represented by each cluster. Subsequently, we conducted gene co-expression network analysis (WGCNA) separately on the global samples and the clustered samples, resulting in global modules and cluster-specific modules. Comparative analyses of global modules and cluster-specific modules have demonstrated that cluster-specific modules exhibit higher accuracy in co-expression analysis. To measure the degree of condition specificity of genes within condition-specific clusters, we introduced the correlation difference value (CDV). By incorporating the CDV into co-expression analyses, we can assess the condition specificity of genes. This approach proved instrumental in identifying a series of high CDV transcription factor encoding genes upregulated during sustained cold treatment in Camellia sinensis leaves and buds, and pinpointing a pair of genes that participate in the antioxidant defense system of tea plants under sustained cold stress. CONCLUSIONS: To summarize, downsampling and reorganizing the sample set improved the accuracy of co-expression analysis. Cluster-specific modules were more accurate in capturing condition-specific gene interactions. The introduction of CDV allowed for the assessment of condition specificity in gene co-expression analyses. Using this approach, we identified a series of high CDV transcription factor encoding genes related to sustained cold stress in Camellia sinensis. This study highlights the importance of considering condition specificity in co-expression analysis and provides insights into the regulation of the cold stress in Camellia sinensis.

PMID: 38714965


Tree Physiol , IF:4.196 , 2024 May , V44 (5) doi: 10.1093/treephys/tpae040

Transcriptional dynamics reveals the asymmetrical events underlying graft union formation in pecan (Carya illinoinensis).

Mo, Zhenghai and Zhang, Yan and Hou, Mengxin and Hu, Longjiao and Zhai, Min and Xuan, Jiping

Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, NO. 1 Road, Qianhuhou Villiage, Xuanwu District, Nanjing 210014, China.; Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, NO. 1 Road, Qianhuhou Villiage, Xuanwu District, Nanjing 210014, China.; Jiangsu Engineering Research Center for the Germplasm Innovation and Utilization of Pecan, NO. 1 Road, Qianhuhou Villiage, Xuanwu District, Nanjing 210014, China.

Grafting is a widely used technique for pecan propagation; however, the background molecular events underlying grafting are still poorly understood. In our study, the graft partners during pecan [Carya illinoinensis (Wangenh.) K. Koch] graft union formation were separately sampled for RNA-seq, and the transcriptional dynamics were described via weighted gene co-expression network analysis. To reveal the main events underlying grafting, the correlations between modules and grafting traits were analyzed. Functional annotation showed that during the entire graft process, signal transduction was activated in the scion, while messenger RNA splicing was induced in the rootstock. At 2 days after grafting, the main processes occurring in the scion were associated with protein synthesis and processing, while the primary processes occurring in the rootstock were energy release-related. During the period of 7-14 days after grafting, defense response was a critical process taking place in the scion; however, the main process functioning in the rootstock was photosynthesis. From 22 to 32 days after grafting, the principal processes taking place in the scion were jasmonic acid biosynthesis and defense response, whereas the highly activated processes associated with the rootstock were auxin biosynthesis and plant-type secondary cell wall biogenesis. To further prove that the graft partners responded asymmetrically to stress, hydrogen peroxide contents as well as peroxidase and beta-1,3-glucanase activities were detected, and the results showed that their levels were increased in the scion not the rootstock at certain time points after grafting. Our study reveals that the scion and rootstock might respond asymmetrically to grafting in pecan, and the scion was likely associated with stress response, while the rootstock was probably involved in energy supply and xylem bridge differentiation during graft union formation.

PMID: 38598328


Phytopathology , IF:4.025 , 2024 May doi: 10.1094/PHYTO-02-24-0054-KC

From microbes to microbiomes: Applications for plant health and sustainable agriculture.

Beattie, Gwyn A and Bayliss, Kirsty L and Jacobson, Daniel A and Broglie, Richard and Burkett-Cadena, Marleny and Sessitsch, Angela and Kankanala, Prasanna and Stein, Joshua and Eversole, Kellye and Lichens-Park, Ann

Iowa State University, Plant Pathology & Microbiology, 2213 Pammel Drive, 4005 ATRB, Ames, Iowa, United States, 50011-1101; gbeattie@iastate.edu.; Murdoch University, Food Futures Institute, Murdoch, Western Australia, Australia; K.Bayliss@murdoch.edu.au.; Oakridge National Laboratory Biosciences Division, Oakridge, Tennessee, United States; jacobsonda@ornl.gov.; International Alliance for Phytobiomes Research, Eau Claire, Wisconsin, United States; rmbroglie@gmail.com.; Mosaic Biosciences, Plant City, Florida, United States; marleny.burkett@plantresponse.com.; AIT Austrian Institute of Technology, Health & Bioresources Unit, Tulln, Austria; angela.sessitsch@ait.ac.at.; Trace Genomics, Ames, Iowa, United States; prasanna@tracegenomics.com.; Eversole Associates, Bethesda, Maryland, United States; stein@eversoleassociates.com.; Eversole Associates, 5207 Wyoming Road, Bethesda, Maryland, United States, 20816; eversole@eversoleassociates.com.; International Alliance for Phytobiomes Research Inc, Eau Claire, Wisconsin, United States; lichens-park@cox.net.

Plant-microbe interaction research has had a transformative trajectory, from individual microbial isolate studies to comprehensive analyses of plant microbiomes within the broader phytobiome framework. Acknowledging the indispensable role of plant microbiomes in shaping plant health, agriculture, and ecosystem resilience, we underscore the urgent need for sustainable crop production strategies in the face of contemporary challenges. We discuss how the synergies between advancements in 'omics technologies and artificial intelligence can help advance the profound potential of plant microbiomes. Furthermore, we propose a multifaceted approach encompassing translational considerations, transdisciplinary research initiatives, public-private partnerships, regulatory policy development, and pragmatic expectations for the practical application of plant microbiome knowledge across diverse agricultural landscapes. We advocate for strategic collaboration and intentional transdisciplinary efforts to unlock the benefits offered by plant microbiomes and address pressing global issues in food security. By emphasizing a nuanced understanding of plant microbiome complexities and fostering realistic expectations, we encourage the scientific community to navigate the transformative journey from discoveries in the laboratory to field applications. As companies specializing in agricultural microbes and microbiomes undergo shifts, we highlight the necessity of understanding how to approach sustainable agriculture with site-specific management solutions. While cautioning against over-promising, we underscore the excitement of exploring the many impacts of microbiome-plant interactions. We emphasize the importance of collaborative endeavors with societal partners to accelerate our collective capacity to harness the diverse and yet-to-be-discovered beneficial activities of plant microbiomes.

PMID: 38776137


J Sci Food Agric , IF:3.638 , 2024 May , V104 (7) : P4109-4127 doi: 10.1002/jsfa.13293

Integrative metabolome and transcriptome profiling provide insights into elucidation of the synthetic mechanisms of phenolic compounds in Yunnan hulled wheat (Triticum aestivum ssp. yunnanense King).

Zhang, Chuanli and Sha, Yun and Wang, Qianchao and Liu, Junna and Zhang, Ping and Cheng, Shunhe and Qin, Peng

College of Agronomy and Biotechnology, Yunnan Agricultural University, Kunming, China.; College of Tropical Crops, Yunnan Agricultural University, Kunming, China.; Agricultural Technology Extension Station of Lincang, Lincang, China.; Jiangshu Lixiahe Institue of Agriculture Science, Yangzhou, China.

BACKGROUND: Yunnan hulled wheat grains (YHWs) have abundant phenolic compounds (PCs). However, a systematic elucidation of the phenolic characteristics and molecular basis in YHWs is currently lacking. The aim of the study, for the first time, was to conduct metabolomic and transcriptomic analyses of YHWs at different developmental stages. RESULTS: A total of five phenolic metabolite classes (phenolic acids, flavonoids, quinones, lignans and coumarins, and tannins) and 361 PCs were identified, with flavonoids and phenolic acids being the most abundant components. The relative abundance of the identified PCs showed a dynamic decreasing pattern with grain development, and the most significant differences in accumulation were between the enlargement and mature stage, which is consistent with the gene regulation patterns of the corresponding phenolic biosynthesis pathway. Through co-expression and co-network analysis, PAL, HCT, CCR, F3H, CHS, CHI and bZIP were identified and predicted as candidate key enzymes and transcription factors. CONCLUSION: The results broaden our understanding of PC accumulation in wheat whole grains, especially the differential transfer between immature and mature grains. The identified PCs and potential regulatory factors provide important information for future in-depth research on the biosynthesis of PCs and the improvement of wheat nutritional quality. (c) 2024 Society of Chemical Industry.

PMID: 38308467


BMC Microbiol , IF:3.605 , 2024 May , V24 (1) : P153 doi: 10.1186/s12866-024-03307-3

Differences in archaeal diversity and potential ecological functions between saline and hypersaline lakes on Qinghai-Tibet Plateau were driven by multiple environmental and non-environmental factors beyond the salinity.

Wang, Yaqiong and Li, Wenxin and Bao, Guoyuan and Bai, Mohan and Ye, Huike

School of Ecology, Environment and Resources, Qinghai Minzu University, Bayi Road, Xining, 810007, Qinghai, China.; Qinghai Provincial Key Laboratory of High-Value Utilization of Characteristic Economic Plants, Xining, 810007, China.; Qinghai Provincial Biotechnology and Analytical Test Key Laboratory, Xining, 810007, China.; Agro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs / Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, MARA / Tianjin Key Laboratory of Agro-Environment and Agro-Product Safety, Tianjin, 300191, China. baimohan@caas.cn.; Agro-Environmental Protection Institute, Ministry of Agriculture and Rural Affairs / Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, MARA / Tianjin Key Laboratory of Agro-Environment and Agro-Product Safety, Tianjin, 300191, China. yehuike@caas.cn.

BACKGROUND: Saline lakes are home to various archaea that play special and crucial roles in the global biogeochemical cycle. The Qinghai-Tibet Plateau hosts a large number of lakes with diverse salinity ranging from 0.1 to over 400 g/L, harboring complex and diverse archaea. To the best of our knowledge, the formation mechanisms and potential ecological roles of archaea in Qinghai-Tibetan Plateau saline lakes remain largely unknown. RESULTS: Using High-throughput Illumina sequencing, we uncovered the vastly distinct archaea communities between two typical saline lakes with significant salinity differences on the Qinghai Tibet Plateau (Qinghai saline lake and Chaka hypersaline lake) and suggested archaea played different important roles in methanogenesis-related and nitrate reduction-related functions of these two lakes, respectively. Rather than the individual effect of salinity, the composite effect of salinity with diverse environmental parameters (e.g., temperature, chlorophyll a, total nitrogen, and total phosphorus) dominated the explanation of the variations in archaeal community structure in different habitats. Based on the network analysis, we further found the correlations between dominant archaeal OTUs were tight but significantly different between the two habitats, implying that archaeal interactions may also largely determine the shape of archaeal communities. CONCLUSION: The present study improved our understanding of the structure and function of archaea in different saline lakes on the Qinghai-Tibet Plateau and provided a new perspective on the mechanisms underlying shaping their communities.

PMID: 38704527


Enzyme Microb Technol , IF:3.493 , 2024 Jun , V177 : P110429 doi: 10.1016/j.enzmictec.2024.110429

Towards consolidated bioprocessing of biomass and plastic substrates for semi-synthetic production of bio-poly(ethylene furanoate) (PEF) polymer using omics-guided construction of artificial microbial consortia.

Omar, Mohd Norfikri and Minggu, Matthlessa Matthew and Nor Muhammad, Nor Azlan and Abdul, Peer Mohamed and Zhang, Ying and Ramzi, Ahmad Bazli

Institute of Systems Biology (INBIOSIS), Universiti Kebangsaan Malaysia (UKM), UKM, Bangi, Selangor 43600, Malaysia.; Department of Chemical and Process Engineering, Faculty of Engineering and Built Environment, Universiti Kebangsaan Malaysia, Bangi, Selangor 43600, Malaysia; Centre for Sustainable Process Technology (CESPRO), Faculty of Engineering and Built Environment, Universiti Kebangsaan Malaysia, Bangi, Selangor 43600, Malaysia.; BBSRC/EPSRC Synthetic Biology Research Centre (SBRC), School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK.; Institute of Systems Biology (INBIOSIS), Universiti Kebangsaan Malaysia (UKM), UKM, Bangi, Selangor 43600, Malaysia. Electronic address: bazliramzi@ukm.edu.my.

Poly(ethylene furanoate) (PEF) plastic is a 100% renewable polyester that is currently being pursued for commercialization as the next-generation bio-based plastic. This is in line with growing demand for circular bioeconomy and new plastics economy that is aimed at minimizing plastic waste mismanagement and lowering carbon footprint of plastics. However, the current catalytic route for the synthesis of PEF is impeded with technical challenges including high cost of pretreatment and catalyst refurbishment. On the other hand, the semi-biosynthetic route of PEF plastic production is of increased biotechnological interest. In particular, the PEF monomers (Furan dicarboxylic acid and ethylene glycol) can be synthesized via microbial-based biorefinery and purified for subsequent catalyst-mediated polycondensation into PEF. Several bioengineering and bioprocessing issues such as efficient substrate utilization and pathway optimization need to be addressed prior to establishing industrial-scale production of the monomers. This review highlights current advances in semi-biosynthetic production of PEF monomers using consolidated waste biorefinery strategies, with an emphasis on the employment of omics-driven systems biology approaches in enzyme discovery and pathway construction. The roles of microbial protein transporters will be discussed, especially in terms of improving substrate uptake and utilization from lignocellulosic biomass, as well as from depolymerized plastic waste as potential bio-feedstock. The employment of artificial bioengineered microbial consortia will also be highlighted to provide streamlined systems and synthetic biology strategies for bio-based PEF monomer production using both plant biomass and plastic-derived substrates, which are important for circular and new plastics economy advances.

PMID: 38537325


Plant Commun , 2024 May : P100978 doi: 10.1016/j.xplc.2024.100978

Single-cell network analysis reveals gene expression programs for Arabidopsis root development and metabolism.

Han, Ershang and Geng, Zhenxing and Qin, Yue and Wang, Yuewei and Ma, Shisong

MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hefei, China.; MOE Key Laboratory for Cellular Dynamics, School of Life Sciences, Division of Life Sciences and Medicine, University of Science and Technology of China, Innovation Academy for Seed Design, Chinese Academy of Sciences, Hefei, China; School of Data Science, University of Science and Technology of China, Hefei, China. Electronic address: sma@ustc.edu.cn.

Single-cell RNA-seq (scRNA-seq) datasets of Arabidopsis roots have been generated, but related comprehensive gene co-expression network analyses are lacking. We conducted a single-cell gene co-expression network analysis with publicly available scRNA-seq datasets of Arabidopsis roots using a SingleCellGGM algorithm. The analysis identified 149 gene co-expression modules, which we considered gene expression programs (GEPs). By checking their spatiotemporal expression, we identified GEPs specifically expressed in major root cell types along their developmental trajectories. These GEPs defined gene programs regulating root cell development at different stages and are enriched with relevant developmental regulators. As examples, a GEP specific for quiescent center (QC) contains 20 genes regulating QC and stem cell niche homeostasis, and five GEPs are expressed in sieve elements (SEs) from early to late developmental stages, with the early-stage GEP containing 17 known SE developmental regulators. We also identified GEPs for metabolic pathways with cell type-specific expression, suggesting the existence of cell type-specific metabolism in roots. Using the GEPs, we discovered and verified a columella-specific gene, NRL27, as a regulator of auxin-related root gravitropism response. Our analysis thus systematically revealed GEPs regulating Arabidopsis root development and metabolism and provided candidate genes for root biology studies.

PMID: 38783601


Stress Biol , 2024 May , V4 (1) : P25 doi: 10.1007/s44154-024-00162-0

Physiological and molecular bases of the nickel toxicity responses in tomato.

Yu, Hao and Li, Weimin and Liu, Xiaoxiao and Song, Qianqian and Li, Junjun and Xu, Jin

College of Horticulture, Shanxi Agricultural University, Taigu, 030801, China.; Shanxi Key Laboratory of Germplasm Resources Innovation and Utilization of Vegetable and Flower, Taiyuan, 030031, China.; College of Horticulture, Shanxi Agricultural University, Taigu, 030801, China. xujin@sxau.edu.cn.; Shanxi Key Laboratory of Germplasm Resources Innovation and Utilization of Vegetable and Flower, Taiyuan, 030031, China. xujin@sxau.edu.cn.

Nickel (Ni), a component of urease, is a micronutrient essential for plant growth and development, but excess Ni is toxic to plants. Tomato (Solanum lycopersicum L.) is one of the important vegetables worldwide. Excessive use of fertilizers and pesticides led to Ni contamination in agricultural soils, thus reducing yield and quality of tomatoes. However, the molecular regulatory mechanisms of Ni toxicity responses in tomato plants have largely not been elucidated. Here, we investigated the molecular mechanisms underlying the Ni toxicity response in tomato plants by physio-biochemical, transcriptomic and molecular regulatory network analyses. Ni toxicity repressed photosynthesis, induced the formation of brush-like lateral roots and interfered with micronutrient accumulation in tomato seedlings. Ni toxicity also induced reactive oxygen species accumulation and oxidative stress responses in plants. Furthermore, Ni toxicity reduced the phytohormone concentrations, including auxin, cytokinin and gibberellic acid, thereby retarding plant growth. Transcriptome analysis revealed that Ni toxicity altered the expression of genes involved in carbon/nitrogen metabolism pathways. Taken together, these results provide a theoretical basis for identifying key genes that could reduce excess Ni accumulation in tomato plants and are helpful for ensuring food safety and sustainable agricultural development.

PMID: 38722370


Plant Commun , 2024 May , V5 (5) : P100879 doi: 10.1016/j.xplc.2024.100879

Dissecting the molecular basis of spike traits by integrating gene regulatory networks and genetic variation in wheat.

Ai, Guo and He, Chao and Bi, Siteng and Zhou, Ziru and Liu, Ankui and Hu, Xin and Liu, Yanyan and Jin, Liujie and Zhou, JiaCheng and Zhang, Heping and Du, Dengxiang and Chen, Hao and Gong, Xin and Saeed, Sulaiman and Su, Handong and Lan, Caixia and Chen, Wei and Li, Qiang and Mao, Hailiang and Li, Lin and Liu, Hao and Chen, Dijun and Kaufmann, Kerstin and Alazab, Khaled F and Yan, Wenhao

National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China; College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China.; National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China; College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China; Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan 430070, China; Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome, Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China.; National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China.; State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210023, China.; Department for Plant Cell and Molecular Biology, Institute for Biology, Humboldt-Universitat Zu Berlin, 10115 Berlin, Germany.; Plant Research Department, Nuclear Research Center, Egyptian Atomic Energy Authority, Cairo 13759, Egypt.; National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan 430070, China; College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, China. Electronic address: yanwenhao@mail.hzau.edu.cn.

Spike architecture influences both grain weight and grain number per spike, which are the two major components of grain yield in bread wheat (Triticum aestivum L.). However, the complex wheat genome and the influence of various environmental factors pose challenges in mapping the causal genes that affect spike traits. Here, we systematically identified genes involved in spike trait formation by integrating information on genomic variation and gene regulatory networks controlling young spike development in wheat. We identified 170 loci that are responsible for variations in spike length, spikelet number per spike, and grain number per spike through genome-wide association study and meta-QTL analyses. We constructed gene regulatory networks for young inflorescences at the double ridge stage and the floret primordium stage, in which the spikelet meristem and the floret meristem are predominant, respectively, by integrating transcriptome, histone modification, chromatin accessibility, eQTL, and protein-protein interactome data. From these networks, we identified 169 hub genes located in 76 of the 170 QTL regions whose polymorphisms are significantly associated with variation in spike traits. The functions of TaZF-B1, VRT-B2, and TaSPL15-A/D in establishment of wheat spike architecture were verified. This study provides valuable molecular resources for understanding spike traits and demonstrates that combining genetic analysis and developmental regulatory networks is a robust approach for dissection of complex traits.

PMID: 38486454