Nat Commun , IF:14.919 , 2021 Oct , V12 (1) : P5858 doi: 10.1038/s41467-021-26165-3
Integrated omics networks reveal the temporal signaling events of brassinosteroid response in Arabidopsis.
Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.; Department of Genetics, Developmental, and Cell Biology, Iowa State University, Ames, IA, 50011, USA.; Department of Biology, Duke University, Durham, NC, 27708, USA.; Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, 27695, USA.; Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA. jwalley@iastate.edu.
Brassinosteroids (BRs) are plant steroid hormones that regulate cell division and stress response. Here we use a systems biology approach to integrate multi-omic datasets and unravel the molecular signaling events of BR response in Arabidopsis. We profile the levels of 26,669 transcripts, 9,533 protein groups, and 26,617 phosphorylation sites from Arabidopsis seedlings treated with brassinolide (BL) for six different lengths of time. We then construct a network inference pipeline called Spatiotemporal Clustering and Inference of Omics Networks (SC-ION) to integrate these data. We use our network predictions to identify putative phosphorylation sites on BES1 and experimentally validate their importance. Additionally, we identify BRONTOSAURUS (BRON) as a transcription factor that regulates cell division, and we show that BRON expression is modulated by BR-responsive kinases and transcription factors. This work demonstrates the power of integrative network analysis applied to multi-omic data and provides fundamental insights into the molecular signaling events occurring during BR response.
PMID: 34615886
Curr Biol , IF:10.834 , 2021 Oct , V31 (20) : P4462-4472.e6 doi: 10.1016/j.cub.2021.07.075
Auxin requirements for a meristematic state in roots depend on a dual brassinosteroid function.
Faculty of Biology, Technion-Israel Institute of Technology, Haifa 3200003, Israel.; Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot, Israel.; Lorey I. Lokey Interdisciplinary Center for Life Sciences and Engineering, Technion-Israel Institute of Technology, Haifa 3200003, Israel.; Laboratory of Growth Regulators, Institute of Experimental Botany, Czech Academy of Sciences and Palacky University, Olomouc, Czech Republic.; Faculty of Biology, Technion-Israel Institute of Technology, Haifa 3200003, Israel. Electronic address: sigal@technion.ac.il.
Root meristem organization is maintained by an interplay between hormone signaling pathways that both interpret and determine their accumulation and distribution. The interacting hormones Brassinosteroids (BR) and auxin control the number of meristematic cells in the Arabidopsis root. BR was reported both to promote auxin signaling input and to repress auxin signaling output. Whether these contradicting molecular outcomes co-occur and what their significance in meristem function is remain unclear. Here, we established a dual effect of BR on auxin, with BR simultaneously promoting auxin biosynthesis and repressing auxin transcriptional output, which is essential for meristem maintenance. Blocking BR-induced auxin synthesis resulted in rapid BR-mediated meristem loss. Conversely, plants with reduced BR levels were resistant to a critical loss of auxin biosynthesis, maintaining their meristem morphology. In agreement, injured root meristems, which rely solely on local auxin synthesis, regenerated when both auxin and BR synthesis were inhibited. Use of BIN2 as a tool to selectively inhibit BR signaling yielded meristems with distinct phenotypes depending on the perturbed tissue: meristem reminiscent either of BR-deficient mutants or of high BR exposure. This enabled mapping of the BR-auxin interaction that maintains the meristem to the outer epidermis and lateral root cap tissues and demonstrated the essentiality of BR signaling in these tissues for meristem response to BR. BR activity in internal tissues however, proved necessary to control BR levels. Together, we demonstrate a basis for inter-tissue coordination and how a critical ratio between these hormones determines the meristematic state.
PMID: 34418341
Plant Physiol , IF:8.34 , 2021 Oct doi: 10.1093/plphys/kiab484
qGL3/OsPPKL1 Induces Phosphorylation of 14-3-3 OsGF14b to Inhibit OsBZR1 Function in Brassinosteroid Signaling.
State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Agriculture, Nanjing Agricultural University, Nanjing 210095, China.; Jiangsu Provincial Engineering Research Center of Seed Industry Science and Technology, Nanjing 210095, China.
Brassinosteroids (BRs) play essential roles in regulating plant growth and development, however, gaps still remain in our understanding of the BR signaling network. We previously cloned a grain length quantitative trait locus qGL3, encoding a rice (Oryza sativa L.) protein phosphatase with Kelch-like repeat domain (OsPPKL1), that negatively regulates grain length and BR signaling. To further explore the BR signaling network, we performed phosphoproteomic analysis to screen qGL3-regulated downstream components. We selected a 14-3-3 protein OsGF14b from the phosphoproteomic data for further analysis. qGL3 promoted the phosphorylation of OsGF14b and induced the interaction intensity between OsGF14b and OsBZR1. In addition, phosphorylation of OsGF14b played an important role in regulating nucleocytoplasmic shuttling of OsBZR1. The serine acids (Ser258Ser259) residues of OsGF14b play an essential role in BR-mediated responses and plant development. Genetic and molecular analyses indicated that OsGF14b functions as a negative regulator in BR signaling and represses the transcriptional activation activity of OsBZR1. Collectively, these results demonstrate that qGL3 induces the phosphorylation of OsGF14b, which modulates nucleocytoplasmic shuttling and transcriptional activation activity of OsBZR1, to eventually negatively regulate BR signaling and grain length in rice.
PMID: 34662408
J Exp Bot , IF:6.992 , 2021 Oct doi: 10.1093/jxb/erab451
Glucose regulates cotton fiber elongation by interacting with brassinosteroid.
State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China.; Collaborative Innovation Center of Henan Grain Crops, Agronomy College, Henan Agricultural University, Zhengzhou 450002, China.; Zhengzhou Research Base, State Key Laboratory of Cotton Biology, Zhengzhou University, Zhengzhou 450001, China.
In plants, glucose (Glc) plays important roles, as a nutrient and signal molecule, in the regulation of growth and development. However, the function of Glc in fiber development of Upland cotton (Gossypium hirsutum) is unclear. Here, using gas chromatography-mass spectrometry (GC-MS), we found that the Glc content in fibers was higher than that in ovules during the fiber elongation stage. In vitro ovule cultures revealed that lower Glc concentrations promoted cotton fiber elongation, while higher concentrations had inhibitory effects. The hexokinase inhibitor N-acetyl-glucosamine (NAG) inhibited cotton fiber elongation in the cultured ovules, indicating that Glc-mediated fiber elongation depends on the Glc signal transduced by hexokinase. RNA sequencing (RNA-seq) analysis and hormone content detection showed that 150 mM Glc significantly activated brassinosteroid (BR) biosynthesis, and the expression of signaling-related genes have also increased, which promoted fiber elongation. And in vitro ovule cultures clarified that BR induced cotton fiber elongation in a dose-dependent manner. In hormone recovery experiments, only BR compensated for the inhibitory effects of NAG on fiber elongation in a Glc-containing medium. However, the ovules cultured with a BR biosynthetic inhibitor brassinazole (BRZ) and from the BR-deficient cotton mutant pag1 had greatly reduced fiber elongation levels at all the tested Glc concentrations, demonstrating that Glc does not compensate for the inhibition of fiber elongation caused by BR biosynthetic defects, which suggested that BR signaling pathway works downstream of Glc during cotton fiber elongation. Altogether, our study showed that Glc occupies an enviable place and crosstalk occurs between Glc and BR signaling during modulation of fiber elongation.
PMID: 34636403
Int J Mol Sci , IF:5.923 , 2021 Oct , V22 (20) doi: 10.3390/ijms222011210
A Sheathed Spike Gene, TaWUS-like Inhibits Stem Elongation in Common Wheat by Regulating Hormone Levels.
Gansu Key Lab of Crop Improvement and Germplasm Enhancement, College of Agronomy, Gansu Agricultural University, Lanzhou 730070, China.; Key Laboratory of Crop Gene Resources and Germplasm Enhancement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China.
The elongation and development of wheat (Triticum aestivum L.) stem play an important role in plant architecture. The shortened stem would result in a sheathed spike and a low yield in crops. Unraveling the molecular mechanisms underlying a sheathed spike would be beneficial for plant architecture and yield improvement. We identified a novel gene, TaWUS-like (WUSCHEL-related homeobox-like), which regulated sheathed spike and plant architecture in wheat. The plant height of overexpression transgenic lines was significantly decreased and the spike was not completely elongated and enclosed in flag leaf sheaths. Moreover, the increase in tiller angle resulted in loose plant architecture and lower yield. The statistical and cytological analysis demonstrated that the length of the uppermost and secondary internode was significantly shortened, especially the uppermost internode which was only half the length of the wild-type. The size of parenchyma cells was obviously reduced and cell length on the longitudinal section was elongated insufficiently compared with wild-type. The analysis of hormone content showed that there was a lack of gibberellin A 3 (GA3) in internodes but a higher brassinosteroid (BR) content. TaWUS-like may inhibit the synthesis of GA3 and/or BR, thus affecting the function of signal transduction of these hormones, which further caused stem shortening and plant dwarfing in wheat.
PMID: 34681870
J Cell Sci , IF:5.285 , 2021 Oct , V134 (20) doi: 10.1242/jcs.259134
Phosphorylation-dependent routing of RLP44 towards brassinosteroid or phytosulfokine signalling.
Centre for Organismal Studies Heidelberg, University of Heidelberg, INF230, 69120 Heidelberg, Germany.; Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS), Shanghai 201602China.; Department of Plant Biochemistry, Centre for Plant Molecular Biology (ZMBP), Eberhard Karls University, D-72076 Tubingen, Germany.
Plants rely on cell surface receptors to integrate developmental and environmental cues into behaviour adapted to the conditions. The largest group of these receptors, leucine-rich repeat receptor-like kinases, form a complex interaction network that is modulated and extended by receptor-like proteins. This raises the question of how specific outputs can be generated when receptor proteins are engaged in a plethora of promiscuous interactions. RECEPTOR-LIKE PROTEIN 44 (RLP44) acts to promote both brassinosteroid and phytosulfokine signalling, which orchestrate diverse cellular responses. However, it is unclear how these activities are coordinated. Here, we show that RLP44 is phosphorylated in its highly conserved cytosolic tail and that this post-translational modification governs its subcellular localization. Whereas phosphorylation is essential for brassinosteroid-associated functions of RLP44, its role in phytosulfokine signalling is not affected by phospho-status. Detailed mutational analysis suggests that phospho-charge, rather than modification of individual amino acids determines routing of RLP44 to its target receptor complexes, providing a framework to understand how a common component of different receptor complexes can get specifically engaged in a particular signalling pathway.
PMID: 34569597
Plant Mol Biol , IF:4.076 , 2021 Oct doi: 10.1007/s11103-021-01199-9
Different regulatory mechanisms of plant hormones in the ripening of climacteric and non-climacteric fruits: a review.
School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, People's Republic of China.; College of Light Industry and Food Engineering, Nanjing Forestry University, Nanjing, 210037, People's Republic of China.; School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, People's Republic of China. zhhxue@tju.edu.cn.
KEY MESSAGE: This review contains the regulatory mechanisms of plant hormones in the ripening process of climacteric and non-climacteric fruits, interactions between plant hormones and future research directions. The fruit ripening process involves physiological and biochemical changes such as pigment accumulation, softening, aroma and flavor formation. There is a great difference in the ripening process between climacteric fruits and non-climacteric fruits. The ripening of these two types of fruits is affected by endogenous signals and exogenous environments. Endogenous signaling plant hormones play an important regulatory role in fruit ripening. This paper systematically reviews recent progress in the regulation of plant hormones in fruit ripening, including ethylene, abscisic acid, auxin, jasmonic acid (JA), gibberellin, brassinosteroid (BR), salicylic acid (SA) and melatonin. The role of plant hormones in both climacteric and non-climacteric fruits is discussed, with emphasis on the interaction between ethylene and other adjustment factors. Specifically, the research progress and future research directions of JA, SA and BR in fruit ripening are discussed, and the regulatory network between JA and other signaling molecules remains to be further revealed. This study is meant to expand the understanding of the importance of plant hormones, clarify the hormonal regulation network and provide a basis for targeted manipulation of fruit ripening.
PMID: 34633626
Plant Direct , IF:3.038 , 2021 Oct , V5 (10) : Pe340 doi: 10.1002/pld3.340
Brassinosteroids promote parenchyma cell and secondary xylem development in sugar beet (Beta vulgaris L.) root.
Sugar Beet Physiological Research Institute Inner Mongolia Agricultural University Hohhot China.
Increasing crop yield has always been an important goal in agriculture. Brassinosteroids (BRs) are growth-promoting steroid hormones with vital roles in many root developmental processes. Sugar beet (Beta vulgaris L.) is a root crop with a tertiary root structure. The differentiation of vascular bundles and the division of cambial cells increase root diameter. However, little is known about how BRs regulate the transverse growth of beetroot. Therefore, sugar beet with eight leaves was grown in medium containing epibrassinolide or brassinazole, an inhibitor of BR biosynthesis. BRs increased the spacing between the cambial rings by increasing the size of parenchyma cells between the rings and ultimately increasing root diameter. BRs also promoted secondary xylem differentiation. Moreover, the gene expression analysis of BvXTH33, BvSHV3, BvCESA6, BvPARVUS, and BvCEL1, which were related to the cell wall biosynthesis, indicated that BR could promote the growth of cell wall. These findings showed that BRs function in transverse development in beetroot.
PMID: 34693195