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Autophagy , IF:16.016 , 2021 Nov , V17 (11) : P3375-3388 doi: 10.1080/15548627.2021.1872886

ATI1 (ATG8-interacting protein 1) and ATI2 define a plant starvation-induced reticulophagy pathway and serve as MSBP1/MAPR5 cargo receptors.

Wu, Jian and Michaeli, Simon and Picchianti, Lorenzo and Dagdas, Yasin and Galili, Gad and Peled-Zehavi, Hadas

Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel.; Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria.

Reticulophagy, the selective autophagy of endoplasmic reticulum (ER) components, is known to operate in eukaryotes from yeast and unicellular algae to animals and plants. Thus far, only ER-stress induced reticulophagy was reported and analyzed in plants. In this study we characterize a reticulophagy pathway in Arabidopsis thaliana that is triggered by dark-induced starvation but not by ER stress. This pathway is defined by the previously reported ATG8-interacting proteins, ATI1 and ATI2. We further identified the ER-localized MSBP1 (Membrane Steroid Binding Protein 1) as an ATI1- and ATI2-interacting protein and an autophagy cargo, and show that ATI1 and ATI2 serve as its cargo receptors. Together, these findings expand our knowledge on plant responses during energy deprivation and highlight the role of this special type of reticulophagy in this process.Abbreviations: AGO1: ARGONAUTE 1; ATI: ATG8-Interacting Protein; BiFC: Bimolecular Fluorescence Complementation; BR: brassinosteroid; conA: concanamycin A; DMSO: dimethyl sulfoxid; DTT: dithiothreitol; ER: endoplasmic reticulum; GFP: green fluorescent protein; MAPR: Membrane-Associated Progesterone Binding Protein; MSBP: Membrane Steroid Binding Protein; SD: standard deviation; SE: standard error; TM: tunicamycin; TOR: target of rapamycin; Y2H: yeast two-hybrid.

PMID: 33487099


Nat Plants , IF:15.793 , 2021 Nov , V7 (11) : P1475-1484 doi: 10.1038/s41477-021-01014-9

The root meristem is shaped by brassinosteroid control of cell geometry.

Fridman, Y and Strauss, S and Horev, G and Ackerman-Lavert, M and Reiner-Benaim, A and Lane, B and Smith, R S and Savaldi-Goldstein, S

Faculty of Biology, Technion-Israel Institute of Technology, Haifa, Israel.; Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.; Lorey I. Lokey Interdisciplinary Center for Life Sciences and Engineering, Technion - Israel Institute of Technology, Haifa, Israel.; Clinical Epidemiology Unit, Rambam Health Care Campus, Haifa, Israel.; Department of Computational and Systems Biology, John Innes Centre, Norwich, UK.; Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany. richard.smith@jic.ac.uk.; Department of Computational and Systems Biology, John Innes Centre, Norwich, UK. richard.smith@jic.ac.uk.; Faculty of Biology, Technion-Israel Institute of Technology, Haifa, Israel. sigal@technion.ac.il.

Growth extent and direction determine cell and whole-organ architecture. How they are spatio-temporally modulated to control size and shape is not well known. Here we tackled this question by studying the effect of brassinosteroid (BR) signalling on the structure of the root meristem. Quantification of the three-dimensional geometry of thousands of individual meristematic cells across different tissue types showed that the modulation of BR signalling yields distinct changes in growth rate and anisotropy, which affects the time that cells spend in the meristem and has a strong impact on the final root form. By contrast, the hormone effect on cell volume was minor, establishing cell volume as invariant to the effect of BR. Thus, BR has the highest effect on cell shape and growth anisotropy, regulating the overall longitudinal and radial growth of the meristem, while maintaining a coherent distribution of cell sizes. Moving from single-cell quantification to the whole organ, we developed a computational model of radial growth. The simulation demonstrates how differential BR-regulated growth between the inner and outer tissues shapes the meristem and thus explains the non-intuitive outcomes of tissue-specific perturbation of BR signalling. The combined experimental data and simulation suggest that the inner and outer tissues have distinct but coordinated roles in growth regulation.

PMID: 34782771


Mol Plant , IF:13.164 , 2021 Nov , V14 (11) : P1935-1950 doi: 10.1016/j.molp.2021.07.016

Suppression of LjBAK1-mediated immunity by SymRK promotes rhizobial infection in Lotus japonicus.

Feng, Yong and Wu, Ping and Liu, Chao and Peng, Liwei and Wang, Tao and Wang, Chao and Tan, Qian and Li, Bixuan and Ou, Yajuan and Zhu, Hui and Yuan, Songli and Huang, Renliang and Stacey, Gary and Zhang, Zhongming and Cao, Yangrong

State Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, and College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China.; Divisions of Plant Sciences and Biochemistry, C. S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA.; State Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, and College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China. Electronic address: yrcao@mail.hzau.edu.cn.

An important question in biology is how organisms can associate with different microbes that pose no threat (commensals), pose a severe threat (pathogens), and those that are beneficial (symbionts). The root nodule symbiosis serves as an important model system for addressing such questions in the context of plant-microbe interactions. It is now generally accepted that rhizobia can actively suppress host immune responses during the infection process, analogous to the way in which plant pathogens can evade immune recognition. However, much remains to be learned about the mechanisms by which the host recognizes the rhizobia as pathogens and how, subsequently, these pathways are suppressed to allow establishment of the nitrogen-fixing symbiosis. In this study, we found that SymRK (Symbiosis Receptor-like Kinase) is required for rhizobial suppression of plant innate immunity in Lotus japonicus. SymRK associates with LjBAK1 (BRASSINOSTEROID INSENSITIVE 1-Associated receptor Kinase 1), a well-characterized positive regulator of plant innate immunity, and directly inhibits LjBAK1 kinase activity. Rhizobial inoculation enhances the association between SymRK and LjBAK1 in planta. LjBAK1 is required for the regulation of plant innate immunity and plays a negative role in rhizobial infection in L. japonicus. The data indicate that the SymRK-LjBAK1 protein complex serves as an intersection point between rhizobial symbiotic signaling pathways and innate immunity pathways, and support that rhizobia may actively suppress the host's ability to mount a defense response during the legume-rhizobium symbiosis.

PMID: 34314895


Plant Cell , IF:11.277 , 2021 Nov , V33 (11) : P3532-3554 doi: 10.1093/plcell/koab210

The F-box E3 ubiquitin ligase BAF1 mediates the degradation of the brassinosteroid-activated transcription factor BES1 through selective autophagy in Arabidopsis.

Wang, Ping and Nolan, Trevor M and Clark, Natalie M and Jiang, Hao and Montes-Serey, Christian and Guo, Hongqing and Bassham, Diane C and Walley, Justin W and Yin, Yanhai

Department of Genetics, Development and Cell Biology, Iowa State University, Ames, Iowa 50011.; Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011.; Plant Sciences Institutes, Iowa State University, Ames, Iowa 50011.

Brassinosteroids (BRs) regulate plant growth, development, and stress responses by activating the core transcription factor BRI1-EMS-SUPPRESSOR1 (BES1), whose degradation occurs through the proteasome and autophagy pathways. The E3 ubiquitin ligase(s) that modify BES1 for autophagy-mediated degradation remain to be fully defined. Here, we identified an F-box family E3 ubiquitin ligase named BES1-ASSOCIATED F-BOX1 (BAF1) in Arabidopsis thaliana. BAF1 interacts with BES1 and mediates its ubiquitination and degradation. Our genetic data demonstrated that BAF1 inhibits BR signaling in a BES1-dependent manner. Moreover, BAF1 targets BES1 for autophagic degradation in a selective manner. BAF1-triggered selective autophagy of BES1 depends on the ubiquitin binding receptor DOMINANT SUPPRESSOR OF KAR2 (DSK2). Sucrose starvation-induced selective autophagy of BES1, but not bulk autophagy, was significantly compromised in baf1 mutant and BAF1-DeltaF (BAF1 F-box decoy) overexpression plants, but clearly increased by BAF1 overexpression. The baf1 and BAF1-DeltaF overexpression plants had increased BR-regulated growth but were sensitive to long-term sucrose starvation, while BAF1 overexpression plants had decreased BR-regulated growth but were highly tolerant of sucrose starvation. Our results not only established BAF1 as an E3 ubiquitin ligase that targets BES1 for degradation through selective autophagy pathway, but also revealed a mechanism for plants to reduce growth during sucrose starvation.

PMID: 34436598


Curr Biol , IF:10.834 , 2021 Nov , V31 (21) : P4810-4816.e5 doi: 10.1016/j.cub.2021.08.033

Independent parental contributions initiate zygote polarization in Arabidopsis thaliana.

Wang, Kai and Chen, Houming and Ortega-Perez, Marina and Miao, Yingjing and Ma, Yanfei and Henschen, Agnes and Lohmann, Jan U and Laubinger, Sascha and Bayer, Martin

Max Planck Institute for Developmental Biology, Department of Cell Biology, Max-Planck-Ring 5, 72076 Tubingen, Germany.; Centre for Organismal Studies, Heidelberg University, Department of Stem Cell Biology, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany.; University of Oldenburg, Institute for Biology and Environmental Sciences, Carl-von-Ossietzky-Str. 9-11, 26111 Oldenburg, Germany.; Max Planck Institute for Developmental Biology, Department of Cell Biology, Max-Planck-Ring 5, 72076 Tubingen, Germany. Electronic address: martin.bayer@tuebingen.mpg.de.

Embryogenesis of flowering plants is initiated by polarization of the zygote, a prerequisite for correct axis formation in the embryo. The daughter cells of the asymmetric zygote division form the pro-embryo and the mostly extra-embryonic suspensor.(1) The suspensor plays a pivotal role in nutrient and hormone transport and rapid growth of the embryo.(2)(,)(3) Zygote polarization is controlled by a MITOGEN-ACTIVATING PROTEIN (MAP) kinase signaling pathway including the MAPKK kinase (MAP3K) YODA (YDA)(4) and the upstream membrane-associated proteins BRASINOSTEROID SIGNALING KINASE 1 (BSK1) and BSK2.(5)(,)(6) Furthermore, suspensor development is controlled by cysteine-rich peptides of the EMBRYO SURROUNDING FACTOR 1 (ESF1) family.(7) While they act genetically upstream of YDA, the corresponding receptor to perceive these potential ligands is unknown. In other developmental processes, such as stomata development, YDA activity is controlled by receptor kinases of the ERECTA family (ERf).(8-12) While the receptor kinases upstream of BSK1/2 in the embryo have so far not been identified,(1) YDA is in part activated by the sperm cell-derived BSK family member SHORT SUSPENSOR (SSP) that represents a naturally occurring, constitutively active variant of BSK1.(5)(,)(13) It has been speculated that SSP might be a paternal component of a parental tug-of-war controlling resource allocation toward the embryo.(2)(,)(13) Here, we show that in addition to SSP, the receptor kinase ERECTA plays a crucial role in zygote polarization as a maternally contributed part of the embryonic YDA pathway. We conclude that two independent parental contributions initiate zygote polarization and control embryo development.

PMID: 34496220


New Phytol , IF:10.151 , 2021 Nov doi: 10.1111/nph.17859

GLUTAMATE RECEPTOR-Like gene OsGLR3.4 is required for plant growth and systemic wound signaling in rice (Oryza sativa).

Yu, Bo and Wu, Qi and Li, Xingxing and Zeng, Rongfeng and Min, Qian and Huang, Junli

Key Laboratory of Biorheological Science and Technology of Ministry of Education, Bioengineering College of Chongqing University, 174 Shazheng Street, Chongqing, China.

Recent studies have revealed the physiological roles of glutamate receptor-like channels (GLRs) in Arabidopsis thaliana. Still, the functions of GLRs in rice are largely unknown. Here, we showed that knockout of OsGLR3.4 in rice leads to brassinosteroid (BR)-regulated growth defects and reduced BR sensitivity. Electrophoretic mobility shift assay and transient transactivation assays indicated that OsGLR3.4 is the downstream target of OsBZR1. Further, the agonist profile assays showed that multiple amino acids can trigger transient Ca(2+) influx in an OsGLR3.4-dependent manner, indicating that OsGLR3.4 has the Ca(2+) -permeable channel activity. Meanwhile, the study of internode cells demonstrated that OsGLR3.4-mediated Ca(2+) flux is required for actin filament organization and vesicle trafficking. The root injury triggering slow wave potentials (SWPs) in leaves as well as jasmonic acid (JA) response is impaired in osglr3.4 mutants, indicating that OsGLR3.4 is required for the root-to-shoot systemic wound signaling in rice. BR treatment enhanced SWPs and OsJAZ8 expression in root-wounded plants, suggesting BR signaling synergistically regulated OsGLR3.4-mediated systemic wound response. Together, this work elaborates a mechanism of OsGLR3.4-mediated cell elongation and long-distance systemic wound signaling in plants and provides new insights into the contribution of GLRs to plant growth and mechanical wounding adaption.

PMID: 34767648


Plant Physiol , IF:8.34 , 2021 Nov , V187 (3) : P1284-1285 doi: 10.1093/plphys/kiab413

Intertwined roots: linked nitrate and brassinosteroid signaling pathways modulate root system architecture.

Thiruppathi, Dhineshkumar

Donald Danforth Plant Science Center, Saint Louis, MI 63132, USA.

PMID: 34734287


Plant Physiol , IF:8.34 , 2021 Nov , V187 (3) : P1779-1794 doi: 10.1093/plphys/kiab323

CALMODULIN-LIKE-38 and PEP1 RECEPTOR 2 integrate nitrate and brassinosteroid signals to regulate root growth.

Song, Xiaoyun and Li, Jianfu and Lyu, Mengli and Kong, Xiuzhen and Hu, Shi and Song, Qingwei and Zuo, Kaijing

Plant Biotech Center: Center of Single Cell Research, School of Agriculture and Life Sciences, Shanghai Jiao Tong University, Shanghai 200240, China.

Plants exhibit remarkable developmental plasticity, enabling them to adapt to adverse environmental conditions such as low nitrogen (N) in the soil. Brassinosteroids (BRs) promote root foraging for nutrients under mild N deficiency, but the crosstalk between the BR- and N-signaling pathways in the regulation of root growth remains largely unknown. Here, we show that CALMODULIN-LIKE-38 (CML38), a calmodulin-like protein, specifically interacts with the PEP1 RECEPTOR 2 (PEPR2), and negatively regulates root elongation in Arabidopsis (Arabidopsis thaliana) in response to low nitrate (LN). CML38 and PEPR2 are transcriptionally induced by treatments of exogenous nitrate and BR. Compared with Col-0, the single mutants cml38 and pepr2 and the double mutant cml38 pepr2 displayed enhanced primary root growth and produced more lateral roots under LN. This is consistent with their higher nitrate absorption abilities, and their stronger expression of nitrate assimilation genes. Furthermore, CML38 and PEPR2 regulate common downstream genes related to BR signaling, and they have positive roles in BR signaling. Low N facilitated BR signal transmission in Col-0 and CML38- or PEPR2-overexpressing plants, but not in the cml38 and pepr2 mutants. Taken together, our results illustrate a mechanism by which CML38 interacts with PEPR2 to integrate LN and BR signals for coordinating root development to prevent quick depletion of N resources in Arabidopsis.

PMID: 34618046


Environ Pollut , IF:8.071 , 2021 Nov , V293 : P118510 doi: 10.1016/j.envpol.2021.118510

Roles of exogenous plant growth regulators on phytoextraction of Cd/Pb/Zn by Sedum alfredii Hance in contaminated soils.

Chen, Zhiqin and Liu, Qizhen and Chen, Shaoning and Zhang, Shijun and Wang, Mei and Mujtaba Munir, Mehr Ahmed and Feng, Ying and He, Zhenli and Yang, Xiaoe

MOE Key Laboratory of Environment Remediation and Ecological Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, People's Republic of China.; College of Life Sciences and Medicine, Zhejiang Sci-Tech University, Hangzhou, 310018, People's Republic of China.; University of Florida, Institute of Food and Agricultural Sciences, Department of Soil and Water Sciences, Indian River Research and Education Center, Fort Pierce, FL, 34945, United States.; MOE Key Laboratory of Environment Remediation and Ecological Health, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, People's Republic of China. Electronic address: xeyang@zju.edu.cn.

Plant growth regulators (PGRs) assisted phytoextraction was investigated as a viable phytoremediation technology to increase the phytoextraction efficiency in contaminated soils. This study aimed to evaluate the cadimum (Cd)/lead (Pb)/zinc (Zn) phytoextraction efficiency by a hyperaccumulator Sedum alfredii Hance (S. alfredii) treated with 9 PGRs, including indole-3-acetic acid (IAA), gibberellin (GA3), cytokinin (CKs), abscisic acid (ABA), ethylene (ETH), brassinosteroid (BR), salicylic acid (SA), strigolactones (SL) and jasmonic acid (JA), in slightly or heavily contaminated (SC and HC, respectively) soil. Results demonstrated that PGRs were able to improve S. alfredii biomass, the most significant increases were observed in GA3 and SL for HC soil, while for SC soil, IAA and BR exhibited positive effects. The levels of Cd, Pb and Zn in the shoots of S. alfredii treated with ABA and SL were noticeably greater than in the CK treatment in HC soil, while the uptake of metals were increased by IAA and CKs in SC soil. Combined with the results of biomass and metal contents in shoots, we found that ABA showed the highest Cd removal efficiency and the maximum Pb and Zn removal efficiency was observed with GA3, which was 62.99%, 269.23%, and 41.18%, respectively higher than the control in HC soil. Meanwhile, compared to control, the maximum removal efficiency of Cd by IAA treatment (52.80%), Pb by JA treatment (165.1%), and Zn by BR treatment (44.97%) in the SC soil. Overall, our results suggested that these PGRs, especially, ABA, SL, IAA, BR and GA3 had great potential in improving phytoremediation efficiency of S. alfredii grown in contaminated soils.

PMID: 34793909


J Integr Plant Biol , IF:7.061 , 2021 Nov doi: 10.1111/jipb.13197

Interaction of brassinosteroid and cytokinin promotes ovule initiation and increases seed number per silique in Arabidopsis.

Zu, Song-Hao and Jiang, Yu-Tong and Chang, Jin-Hui and Zhang, Yan-Jie and Xue, Hong-Wei and Lin, Wen-Hui

School of Life Sciences and Biotechnology, The Joint International Research Laboratory of Metabolic and Developmental Sciences, Joint Center for Single Cell Biology, Shanghai Jiao Tong University, Shanghai, 200240, China.; School of Agriculture and Biology, Joint Center for Single Cell Biology, Shanghai Jiao Tong University, Shanghai, 200240, China.

Ovule initiation is a key step that strongly influences ovule number and seed yield. Notably, mutants with enhanced brassinosteroid (BR) and cytokinin (CK) signaling produce more ovules and have a higher seed number per silique (SNS) than wild-type plants. Here, we crossed BR- and CK-related mutants to test whether these phytohormones function together in ovule initiation. We determined that simultaneously enhancing BR and CK contents led to higher ovule and seed numbers than enhancing BR or CK separately, and BR and CK enhanced each other. Further, the BR-response transcription factor BZR1 directly interacted with the CK-response transcription factor ARABIDOPSIS RESPONSE REGULATOR1 (ARR1). Treatments with BR or BR plus CK strengthened this interaction and subsequent ARR1 targeting and induction of downstream genes to promote ovule initiation. Enhanced CK signaling partially rescued the reduced SNS phenotype of BR-deficient/insensitive mutants whereas enhanced BR signaling failed to rescue the low SNS of CK-deficient mutants, suggesting that BR regulates ovule initiation and SNS through CK-mediated and CK-independent pathways. Our study thus reveals that interaction between BR and CK promotes ovule initiation and increases seed number, providing important clues for increasing the seed yield of dicot crops. This article is protected by copyright. All rights reserved.

PMID: 34837335


Development , IF:6.868 , 2021 Nov , V148 (21) doi: 10.1242/dev.199504

Optimal BR signalling is required for adequate cell wall orientation in the Arabidopsis root meristem.

Li, Zhenni and Sela, Ayala and Fridman, Yulia and Garstka, Lucia and Hofte, Herman and Savaldi-Goldstein, Sigal and Wolf, Sebastian

Department of Cell Biology, Centre for Organismal Studies Heidelberg, Heidelberg University, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany.; Plant Biology Laboratory, Technion-Israel Institute of Technology, Haifa 3200003, Israel.; Department of Development, Signalling, and Modelling, Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Universite Paris-Saclay, 78000 Versailles, France.; Department of Plant Biochemistry, Centre for Plant Molecular Biology (ZMBP), Eberhard Karls University, D-72076 Tubingen, Germany.

Plant brassinosteroid hormones (BRs) regulate growth in part through altering the properties of the cell wall, the extracellular matrix of plant cells. Conversely, feedback signalling from the wall connects the state of cell wall homeostasis to the BR receptor complex and modulates BR activity. Here, we report that both pectin-triggered cell wall signalling and impaired BR signalling result in altered cell wall orientation in the Arabidopsis root meristem. Furthermore, both depletion of endogenous BRs and exogenous supply of BRs triggered these defects. Cell wall signalling-induced alterations in the orientation of newly placed walls appear to occur late during cytokinesis, after initial positioning of the cortical division zone. Tissue-specific perturbations of BR signalling revealed that the cellular malfunction is unrelated to previously described whole organ growth defects. Thus, tissue type separates the pleiotropic effects of cell wall/BR signals and highlights their importance during cell wall placement.

PMID: 34739031


Ann Bot , IF:4.357 , 2021 Nov , V128 (7) : P931-942 doi: 10.1093/aob/mcab116

Brassinosteroids regulate petal spur length in Aquilegia by controlling cell elongation.

Conway, Stephanie J and Walcher-Chevillet, Cristina L and Salome Barbour, Kate and Kramer, Elena M

Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Ave., Cambridge, MA 02138, USA.; 10x Genomics Inc., 6230 Stoneridge Mall Road, Pleasanton, CA 94588, USA.; Abramson Cancer Center, University of Pennsylvania, 3400 Civic Center Blvd., Philadelphia, PA 19104, USA.

BACKGROUND AND AIMS: Aquilegia produce elongated, three-dimensional petal spurs that fill with nectar to attract pollinators. Previous studies have shown that the diversity of spur length across the Aquilegia genus is a key innovation that is tightly linked with its recent and rapid diversification into new ranges, and that evolution of increased spur lengths is achieved via anisotropic cell elongation. Previous work identified a brassinosteroid response transcription factor as being enriched in the early developing spur cup. Brassinosteroids are known to be important for cell elongation, suggesting that brassinosteroid-mediated response may be an important regulator of spur elongation and potentially a driver of spur length diversity in Aquilegia. In this study, we investigated the role of brassinosteroids in the development of the Aquilegia coerulea petal spur. METHODS: We exogenously applied the biologically active brassinosteroid brassinolide to developing petal spurs to investigate spur growth under high hormone conditions. We used virus-induced gene silencing and gene expression experiments to understand the function of brassinosteroid-related transcription factors in A. coerulea petal spurs. KEY RESULTS: We identified a total of three Aquilegia homologues of the BES1/BZR1 protein family and found that these genes are ubiquitously expressed in all floral tissues during development, yet, consistent with the previous RNAseq study, we found that two of these paralogues are enriched in early developing petals. Exogenously applied brassinosteroid increased petal spur length due to increased anisotropic cell elongation as well as cell division. We found that targeting of the AqBEH genes with virus-induced gene silencing resulted in shortened petals, a phenotype caused in part by a loss of cell anisotropy. CONCLUSIONS: Collectively, our results support a role for brassinosteroids in anisotropic cell expansion in Aquilegia petal spurs and highlight the brassinosteroid pathway as a potential player in the diversification of petal spur length in Aquilegia.

PMID: 34508638


BMC Plant Biol , IF:4.215 , 2021 Nov , V21 (1) : P543 doi: 10.1186/s12870-021-03332-8

Genome-wide identification of Gramineae histone modification genes and their potential roles in regulating wheat and maize growth and stress responses.

Zheng, Liwei and Ma, Shengjie and Shen, Dandan and Fu, Hong and Wang, Yue and Liu, Ying and Shah, Kamran and Yue, Caipeng and Huang, Jinyong

School of Agricultural Sciences, Zhengzhou University, Henan, 450001, China.; College of Horticulture, Northwest A & F University, Yangling, 712100, Shaanxi, China.; School of Agricultural Sciences, Zhengzhou University, Henan, 450001, China. jinyhuang@zzu.edu.cn.

BACKGROUND: In plants, histone modification (HM) genes participate in various developmental and defense processes. Gramineae plants (e.g., Triticum aestivum, Hordeum vulgare, Sorghum bicolor, Setaria italica, Setaria viridis, and Zea mays) are important crop species worldwide. However, little information on HM genes is in Gramineae species. RESULTS: Here, we identified 245 TaHMs, 72 HvHMs, 84 SbHMs, 93 SvHMs, 90 SiHMs, and 90 ZmHMs in the above six Gramineae species, respectively. Detailed information on their chromosome locations, conserved domains, phylogenetic trees, synteny, promoter elements, and gene structures were determined. Among the HMs, most motifs were conserved, but several unique motifs were also identified. Our results also suggested that gene and genome duplications potentially impacted the evolution and expansion of HMs in wheat. The number of orthologous gene pairs between rice (Oryza sativa) and each Gramineae species was much greater than that between Arabidopsis and each Gramineae species, indicating that the dicotyledons shared common ancestors. Moreover, all identified HM gene pairs likely underwent purifying selection based on to their non-synonymous (Ka)/synonymous (Ks) nucleotide substitutions. Using published transcriptome data, changes in TaHM gene expression in developing wheat grains treated with brassinosteroid, brassinazole, or activated charcoal were investigated. In addition, the transcription models of ZmHMs in developing maize seeds and after gibberellin treatment were also identified. We also examined plant stress responses and found that heat, drought, salt, insect feeding, nitrogen, and cadmium stress influenced many TaHMs, and drought altered the expression of several ZmHMs. Thus, these findings indicate their important functions in plant growth and stress adaptations. CONCLUSIONS: Based on a comprehensive analysis of Gramineae HMs, we found that TaHMs play potential roles in grain development, brassinosteroid- and brassinazole-mediated root growth, activated charcoal-mediated root and leaf growth, and biotic and abiotic adaptations. Furthermore, ZmHMs likely participate in seed development, gibberellin-mediated leaf growth, and drought adaptation.

PMID: 34800975


BMC Plant Biol , IF:4.215 , 2021 Nov , V21 (1) : P510 doi: 10.1186/s12870-021-03283-0

Genome and transcriptome-based characterization of high energy carbon-ion beam irradiation induced delayed flower senescence mutant in Lotus japonicus.

Du, Yan and Luo, Shanwei and Zhao, Jian and Feng, Zhuo and Chen, Xia and Ren, Weibin and Liu, Xiao and Wang, Zhuanzi and Yu, Lixia and Li, Wenjian and Qu, Ying and Liu, Jie and Zhou, Libin

Biophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, 730000, Lanzhou, People's Republic of China.; University of Chinese Academy of Sciences, Beijing, 100000, People's Republic of China.; Guangdong Key Laboratory for New Technology Research of Vegetables, Vegetable Research Institute, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, Guangdong, China.; School of Life Science and Engineering, Lanzhou University of Technology, Lanzhou, 730000, People's Republic of China.; Kejin Innovation Institute of Heavy Ion Beam Biological Industry, Baiyin, 730900, People's Republic of China.; Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100000, People's Republic of China.; Biophysics Group, Biomedical Center, Institute of Modern Physics, Chinese Academy of Sciences, 730000, Lanzhou, People's Republic of China. libinzhou@impcas.ac.cn.; University of Chinese Academy of Sciences, Beijing, 100000, People's Republic of China. libinzhou@impcas.ac.cn.; Kejin Innovation Institute of Heavy Ion Beam Biological Industry, Baiyin, 730900, People's Republic of China. libinzhou@impcas.ac.cn.

BACKGROUND: Flower longevity is closely related to pollen dispersal and reproductive success in all plants, as well as the commercial value of ornamental plants. Mutants that display variation in flower longevity are useful tools for understanding the mechanisms underlying this trait. Heavy-ion beam irradiation has great potential to improve flower shapes and colors; however, few studies are available on the mutation of flower senescence in leguminous plants. RESULTS: A mutant (C416) exhibiting blossom duration eight times longer than that of the wild type (WT) was isolated in Lotus japonicus derived from carbon ion beam irradiation. Genetic assays supported that the delayed flower senescence of C416 was a dominant trait controlled by a single gene, which was located between 4,616,611 Mb and 5,331,876 Mb on chromosome III. By using a sorting strategy of multi-sample parallel genome sequencing, candidate genes were narrowed to the gene CUFF.40834, which exhibited high identity to ethylene receptor 1 in other model plants. A physiological assay demonstrated that C416 was insensitive to ethylene precursor. Furthermore, the dynamic changes of phytohormone regulatory network in petals at different developmental stages was compared by using RNA-seq. In brief, the ethylene, jasmonic acid (JA), and salicylic acid (SA) signaling pathways were negatively regulated in C416, whereas the brassinosteroid (BR) and cytokinin signaling pathways were positively regulated, and auxin exhibited dual effects on flower senescence in Lotus japonicus. The abscisic acid (ABA) signaling pathway is positively regulated in C416. CONCLUSION: So far, C416 might be the first reported mutant carrying a mutation in an endogenous ethylene-related gene in Lotus japonicus, rather than through the introduction of exogenous genes by transgenic techniques. A schematic of the flower senescence of Lotus japonicus from the perspective of the phytohormone regulatory network was provided based on transcriptome profiling of petals at different developmental stages. This study is informative for elucidating the molecular mechanism of delayed flower senescence in C416, and lays a foundation for candidate flower senescence gene identification in Lotus japonicus. It also provides another perspective for the improvement of flower longevity in legume plants by heavy-ion beam.

PMID: 34732128


Plant Genome , IF:4.089 , 2021 Nov : Pe20174 doi: 10.1002/tpg2.20174

Genome-wide association study for lignocellulosic compounds and fermentable sugar in rice straw.

Panahabadi, Rahele and Ahmadikhah, Asadollah and McKee, Lauren S and Ingvarsson, Par K and Farrokhi, Naser

Faculty of Life Sciences and Biotechnology, Shahid Beheshti Univ., Tehran, Iran.; Division of Glycoscience, School of Biotechnology, Royal Institute of Technology (KTH), AlbaNova University Centre, Stockholm, 106 91, Sweden.; Wallenberg Wood Science Centre, Teknikringen 56-58, Stockholm, 100 44, Sweden.; Linnean Centre for Plant Biology, Dep. of Plant Biology, Swedish Univ. of Agricultural Sciences, Uppsala, Sweden.

Cellulose and lignin are the two main components of secondary plant cell walls with substantial impact on stalk in the field and on straw during industrial processing. The amount of fermentable sugar that can be accessed is another important parameter affecting various industrial applications. In the present study, genetic variability of rice (Oryza sativa L.) genotypes for cellulose, lignin, and fermentable sugars contents was analyzed in rice straw. A genome-wide association study of 33,484 single nucleotide polymorphisms (SNPs) with a minor allele frequency (MAF) >0.05 was performed. The genome-wide association study identified seven, three, and three genomic regions to be significantly associated with cellulose, lignin, and fermentable sugar contents, respectively. Candidate genes in the associated genomic regions were enzymes mainly involved in cell wall metabolism. Novel SNP markers associated with cellulose were tagged to GH16, peroxidase, GT6, GT8, and CSLD2. For lignin content, Villin protein, OsWAK1/50/52/53, and GH16 were identified. For fermentable sugar content, UTP-glucose-1-phosphate uridylyltransferase, BRASSINOSTEROID INSENSITIVE 1, and receptor-like protein kinase 5 were found. The results of this study should improve our understanding of the genetic basis of the factors that might be involved in biosynthesis, turnover, and modification of major cell wall components and saccharides in rice straw.

PMID: 34806838


Plants (Basel) , IF:3.935 , 2021 Nov , V10 (11) doi: 10.3390/plants10112484

Comparative Transcriptomic Analysis Provides Novel Insights into the Blanched Stem of Oenanthe javanica.

Kumar, Sunjeet and Huang, Xinfang and Li, Gaojie and Ji, Qun and Zhou, Kai and Zhu, Guopeng and Ke, Weidong and Hou, Hongwei and Zhu, Honglian and Yang, Jingjing

The State Key Laboratory of Freshwater Ecology and Biotechnology, The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China.; University of Chinese Academy of Sciences, Beijing 100049, China.; Key Laboratory for Quality Regulation of Tropical Horticultural Crops of Hainan Province, Engineering Research Center of the Ministry of Education for New Variety Breeding of Tropical Crop, School of Horticulture, Hainan University, Haikou 570228, China.; Institute of Vegetables, Wuhan Academy of Agricultural Sciences, Wuhan 430207, China.

In the agricultural field, blanching is a technique used to obtain tender, sweet, and delicious water dropwort stems by blocking sunlight. The physiological and nutritional parameters of blanched water dropwort have been previously investigated. However, the molecular mechanism of blanching remains unclear. In the present study, we investigated transcriptomic variations for different blanching periods in the stem of water dropwort (pre, mid, post-blanching, and control). The results showed that many genes in pathways, such as photosynthesis, carbon fixation, and phytohormone signal transduction as well as transcription factors (TFs) were significantly dysregulated. Blanched stems of water dropwort showed the higher number of downregulated genes in pathways, such as photosynthesis, antenna protein, carbon fixation in photosynthetic organisms, and porphyrin and chlorophyll metabolism, which ultimately affect the photosynthesis in water dropwort. The genes of hormone signal transduction pathways (ethylene, jasmonic acid, brassinosteroid, and indole-3-acetic acid) showed upregulation in the post-blanched water dropwort plants. Overall, a higher number of genes coding for TFs, such as ERF, BHLH, MYB, zinc-finger, bZIP, and WRKY were overexpressed in blanched samples in comparison with the control. These genes and pathways participate in inducing the length, developmental processes, pale color, and stress tolerance of the blanched stem. Overall, the genes responsive to blanching, which were identified in this study, provide an effective foundation for further studies on the molecular mechanisms of blanching and photosynthesis regulations in water dropwort and other species.

PMID: 34834849


Biochem Biophys Res Commun , IF:3.575 , 2021 Dec , V585 : P117-123 doi: 10.1016/j.bbrc.2021.11.042

Sheath blight resistance in rice is negatively regulated by WRKY53 via SWEET2a activation.

Gao, Yue and Xue, Cai Yun and Liu, Jing Miao and He, Ying and Mei, Qiong and Wei, Songhong and Xuan, Yuan Hu

College of Plant Protection, Shenyang Agricultural University, Shenyang, 110866, China. Electronic address: gaoyue@stu.syau.edu.cn.; College of Plant Protection, Shenyang Agricultural University, Shenyang, 110866, China. Electronic address: syauxue@syau.edu.cn.; Southern Zhejiang Key Laboratory of Crop Breeding, Wenzhou Vocational College of Science and Technology (Wenzhou Academy of Agricultural Sciences), Wenzhou, Zhejiang, 325006, China. Electronic address: liujingmiao@hotmail.com.; Foreign Language Teaching Department, Shenyang Agricultural University, Shenyang, 110866, China. Electronic address: 1994500028@syau.edu.cn.; College of Plant Protection, Shenyang Agricultural University, Shenyang, 110866, China. Electronic address: meiqiong@syau.edu.cn.; College of Plant Protection, Shenyang Agricultural University, Shenyang, 110866, China. Electronic address: songhongw125@163.com.; College of Plant Protection, Shenyang Agricultural University, Shenyang, 110866, China. Electronic address: xuanyuanhu115@syau.edu.cn.

Sheath blight (ShB) is one of the most common diseases in rice that significantly affects yield production. However, the underlying mechanisms of rice defense remain largely unknown. Our previous transcriptome analysis identified that infection with Rhizoctonia solani significantly induced the expression level of SWEET2a, a member of the SWEET sugar transporter. The sweet2a genome-editing mutants were less susceptible to ShB. Further yeast-one hybrid, ChIP, and transient assays demonstrated that WRKY53 binds to the SWEET2a promoter to activate its expression. WRKY53 is a key brassinosteroid (BR) signaling transcription factor. Similar to the BR receptor gene BRI1 and biosynthetic gene D2 mutants, the WRKY53 mutant and overexpressor were less and more susceptible to ShB compared to wild-type, respectively. Inoculation with R. solani induced expression of BRI1, D2, and WRKY53, but inhibited MPK6 (a BR-signaling regulator) activity. Also, MPK6 is known to phosphorylate WRKY53 to enhance its transcription activation activity. Transient assay results indicated that co-expression of MPK6 and WRKY53 enhanced WRKY53 trans-activation activity to SWEET2a. Furthermore, expression of WRKY53 SD (the active phosphorylated forms of WRKY53) but not WRKY53 SA (the inactive phosphorylated forms of WRKY53), enhanced WRKY53-mediated activation of SWEET2a compared to expression of WRKY53 alone. Taken together, our analyses showed that R. solani infection may activate BR signaling to induce SWEET2a expression via WRKY53 through negative regulation of ShB resistance in rice.

PMID: 34801931


Biochem Biophys Res Commun , IF:3.575 , 2021 Nov , V578 : P129-135 doi: 10.1016/j.bbrc.2021.09.035

A bHLH protein, OsBIM1, positively regulates rice leaf angle by promoting brassinosteroid signaling.

Tian, Quanxiang and Luan, Junxia and Guo, Chunxia and Shi, Xingyu and Deng, Ping and Zhou, Zhenzhen and Zhang, Wenhua and Shen, Like

State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China; College of Life and Environmental Science, Hangzhou Normal University, Hangzhou, 311121, China.; State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China.; Excellence and Innovation Center, Jiangsu Academy of Agricultural Science, Nanjing, 210014, China. Electronic address: zhenzhenzhounj@163.com.; State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China. Electronic address: likeshen@njau.edu.cn.

Rice leaf angle is an important agronomic trait determining plant architecture and crop yield. Brassinosteroids (BRs) play crucial roles in controlling rice leaf angle, thus an increasing number of researches were focused on the BR signaling pathway in rice. However, the orthologs of some important components in Arabidopsis BR signaling have not yet been characterized in rice. In this study, we identified a rice bHLH transcription factor named OsBIM1, as the closest rice homolog of AtBIM1 (BES1-Interacting MYC-like Protein1). Overexpression of OsBIM1 significantly increases rice leaf angles, whereas the T-DNA knock-out mutant osbim1 and wide type (WT) showed similar leaf inclination. OsBIM1 overexpression enhances the sensitivity and response to BR treatment in rice. Gene expression analysis showed that the overexpression of OsBIM1 significantly increased the transcripts of INCREASED LEAF INCLINATION1 (OsILI1) that functions as a key transcription factor promoting BR signaling and response. Meanwhile, OsBIM1 inhibited the expression of DWARF2 (OsD2, a key enzyme in BR biosynthesis pathway). OsBIM1 can bind with OsILI1 promoter and enhance OsILI1 expression in response to BR treatment. The promoting effect of OsBIM1 overexpression on leaf angle can still be observed at harvest stage, but overexpression of OsBIM1 resulted in smaller grain size and reduced yield. These results indicate that OsBIM1 functions as a positive regulator in BR signaling, and its overexpression increases rice lamina inclination by promoting BR sensitivity and response.

PMID: 34562652


Plant Signal Behav , IF:2.247 , 2021 Nov , V16 (11) : P1976561 doi: 10.1080/15592324.2021.1976561

Kinase activity is required for the receptor kinase DROOPY LEAF1 to control leaf droopiness.

Wang, Chunfang and Tang, Sha and Zhang, Qi and Shang, Zhonglin and Liu, Xigang and Diao, Xianmin and Zhao, Meicheng

College of Life Sciences, Hebei Normal University, Shijiazhuang, China.; Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China.; School of Biological and Food Science, Hebei Normal University for Nationalities, Chengde, China.; Key Laboratory of Agricultural Water Resources, Hebei Laboratory of Agricultural Water-Saving, Center for Agricultural Resources Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Shijiazhuang, China.

Plants have evolved many leucine-rich repeat receptor-like kinases (LRR-RLKs) that control all aspects of plant life in a kinase-dependent or -independent manner. DROOPY LEAF1 (DPY1), which is a subfamily II LRR-RLK authentic kinase, controls leaf droopiness by negatively regulating early brassinosteroid (BR) signaling in foxtail millet. In this study, we proved that overexpressing kinase-inactive DPY1 does not rescue the droopy leaf phenotype of dpy1 plants because the mutated DPY1 cannot repress BR signaling, suggesting that kinase activity is required for DPY1 to control BR signaling. Moreover, seven DPY1 sites potentially transphosphorylated by SiBAK1 were identified as crucial for DPY1 activation. These findings highlight the importance of kinase activity for the functionality of DPY1.

PMID: 34523390


Plant Signal Behav , IF:2.247 , 2021 Nov , V16 (11) : P1963583 doi: 10.1080/15592324.2021.1963583

24-epibrassinolide confers tolerance against deep-seeding stress in Zea mays L. coleoptile development by phytohormones signaling transduction and their interaction network.

Zhao, Xiaoqiang and Zhong, Yuan and Shi, Jing and Zhou, Wenqi

Gansu Provincial Key Laboratory of Aridland Crop Science/College of Agronomy, Gansu Agricultural University, Lanzhou, P.R. China.; Crop Research Institute, Gansu Academy of Agricultural Sciences, Lanzhou, P.R. China.

Coleoptile/mesocotyl elongation influence seedling emergence and establishment, is major causes of maize deep-seeding tolerance (DST). Detailed analyses on molecular basis underlying their elongation mediated by brassinosteroid under deep-seeding stress (DSS) could provide meaningful information for key factors controlling their elongation. Here we monitored transcriptome and phytohormones changes specifically in elongating coleoptile/mesocotyl in response to DSS and 24-epibrassinolide (EBR)-signaling. Phenotypically, contrasting maize evolved variant organs to positively respond to DST, longer coleoptile/mesocoty of K12/W64A was a desirable organ for seedling under DSS. Applied-EBR improved maize DST, and their coleoptiles/mesocotyls were further elongated. 15,607/20,491 differentially expressed genes (DEGs) were identified in W64A/K12 coleoptile, KEGG analysis showed plant hormone signal transduction, starch and sucrose metabolism, valine, leucine, and isoleucine degradation were critical processes of coleoptile elongation under DSS and EBR signaling, further highly interconnected network maps including 79/142 DEGs for phytohormones were generated. Consistent with these DEGs expression, interactions, and transport, IAA, GA3, ABA, and Cis-ZT were significantly reduced while EBR, Trans-ZT, JA, and SA were clearly increased in coleoptile under DSS and EBR-signaling. These results enrich our knowledge about the genes and phytohormones regulating coleoptile elongation in maize, and help improve future studies on corresponding genes and develop varieties with DST.

PMID: 34425064


Genes Genomics , IF:1.839 , 2021 Nov , V43 (11) : P1269-1276 doi: 10.1007/s13258-021-01148-2

Phosphorylation of BIK1 is critical for interaction with downstream signaling components.

Choi, Jae-Han and Oh, Eun-Seok and Oh, Man-Ho

Department of Biological Sciences, College of Biological Sciences and Biotechnology, Chungnam National University, Daejeon, 34134, Republic of Korea.; Department of Biological Sciences, College of Biological Sciences and Biotechnology, Chungnam National University, Daejeon, 34134, Republic of Korea. manhooh@cnu.ac.kr.

BACKGROUND: Botrytis-induced Kinase 1 (BIK1) is a receptor-like cytoplasmic kinase (RLCK) involved in the defense, growth, and development of higher plants. It interacts with various receptor-like kinases (RLKs) such as Brassinosteroid Insensitive 1 (BRI1), Flagellin Sensitive 2 (FLS2), and Perception of the Arabidopsis Danger Signal Peptide 1 (PEPR1), but little is known about signaling downstream of BIK1. OBJECTIVE: In this study, we aimed to identify Arabidopsis thaliana BIK1 (AtBIK1) and Brassica rapa BIK1 (BrBIK1) interacting proteins, which is downstream signaling components in Arabidopsis. In addition, the effect of BIK1 phosphorylation on their interaction were examined. METHODS: For yeast two hybrid (Y2H) screening, a B. rapa cDNA activation domain (AD) library and an A. thaliana cDNA library were used. Reverse reaction (LR) recombinations of appropriate open reading frames (AtBIK1, BrBIK1, AtRGP2, AtPATL2, AtPP7) in either pDONR207 or pDONR/zeo were performed with the split-YFP destination vectors pDEST-GWVYNE and pDEST-GWVYCE to generate N- or C-terminal fusions with the N- and C-terminal yellow fluorescent protein (YFP) moieties, respectively. Recombined vectors were transformed into Agrobacterium strain GV3101. The described GST-AtBIK1, Flag-AtBIK1, and Flag-BrBIK1 constructs were used as templates for site-directed mutagenesis with a QuikChange XL Site-Directed Mutagenesis Kit (Stratagene). RESULTS: In results, A. thaliana BIK1 (AtBIK1) displays strong autophosphorylation kinase activity on tyrosine and threonine residues, whereas B. rapa BIK1 (BrBIK1) does not exhibit autophosphorylation kinase activity in vitro. Herein, we demonstrated that four proteins (RGP2, PATL2, PP7, and SULTR4.1) interact with BrBIK1 but not AtBIK1 in a Y2H system. To confirm interactions between BIK1 and protein candidates in Nicotiana benthamiana, BiFC analysis was performed and it was found that only BrBIK1 bound the three proteins tested. Three phosphosites, T90, T362, and T368, based on amino acid sequence alignment between AtBIK1 and BrBIK1, and performed site-directed mutagenesis (SDM) on AtBIK1 and BrBIK. S90T, P362T, and A369T mutations in BrBIK1 restored autophosphorylation kinase activity on threonine residues comparable to AtBIK1. However, T90A, T362P, and T368A mutations in AtBIK1 did not alter autophosphorylation kinase activity on threonine residues compared with wild-type AtBIK1. BiFC results showed that BIK1 mutations restored kinase activity led to the loss of the binding activity to RGP2, PATL2, or PP7 proteins. CONCLUSION: Phospho-BIK1 might be involved in plant innate immunity, while non-phospho BIK1 may regulate plant growth and development through interactions with RGP2, PATL2, and PP7.

PMID: 34449065