Dataset Information

EMS1 and BRI1 control separate biological processes via extracellular domain diversity and intracellular domain conservation.

ABSTRACT: In flowering plants, EMS1 (Excess Microsporocytes 1) perceives TPD1 (Tapetum Determinant 1) to specify tapeta, the last somatic cell layer nurturing pollen development. However, the signaling components downstream of EMS1 are relatively unknown. Here, we use a molecular complementation approach to investigate the downstream components in EMS1 signaling. We show that the EMS1 intracellular domain is functionally interchangeable with that of the brassinosteroid receptor BRI1 (Brassinosteroid Insensitive 1). Furthermore, expressing EMS1 together with TPD1 in the BRI1 expression domain could partially rescue bri1 phenotypes, and led to the dephosphorylation of BES1, a hallmark of active BRI1 signaling. Conversely, expressing BRI1 in the EMS1 expression domain could partially rescue ems1 phenotypes. We further show that PpEMS1 and PpTPD1 from the early land plant Physcomitrella patens could completely rescue ems1 and tpd1 phenotypes, respectively. We propose that EMS1 and BRI1 have evolved distinct extracellular domains to control different biological processes but can act via a common intracellular signaling pathway.

SUBMITTER: Zheng B

PROVIDER: S-EPMC6744412 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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EMS1 and BRI1 control separate biological processes via extracellular domain diversity and intracellular domain conservation.

Zheng Bowen B Bai Qunwei Q Wu Lei L Liu Huan H Liu Yuping Y Xu Weijun W Li Guishuang G Ren Hongyan H She Xiaoping X Wu Guang G

Nature communications 20190913 1

In flowering plants, EMS1 (Excess Microsporocytes 1) perceives TPD1 (Tapetum Determinant 1) to specify tapeta, the last somatic cell layer nurturing pollen development. However, the signaling components downstream of EMS1 are relatively unknown. Here, we use a molecular complementation approach to investigate the downstream components in EMS1 signaling. We show that the EMS1 intracellular domain is functionally interchangeable with that of the brassinosteroid receptor BRI1 (Brassinosteroid Insen ...[more]

PMID: 31519884

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Project description:BackgroundSince the identification of BRI1 (BRASSINOSTEROID-INSENSITIVE1), a brassinosteroids (BRs) receptor, most of the critical roles of BR in plant development have been assessed using various bri1 mutant alleles. The characterization of individual bri1 mutants has shown that both the extracellular and cytoplasmic domains of BRI1 are important to its proper functioning. Particularly, in the extracellular domain, regions near the 70-amino acid island are known to be critical to BR binding. In comparison, the exact function of the leucine rich-repeats (LRR) region located before the 70-amino acid island domain in the extracellular cellular portion of BRI1 has not yet been described, due to a lack of specific mutant alleles.ResultsAmong the mutants showing altered growth patterns compared to wild type, we further characterized cp3, which displayed defective growth and reduced BR sensitivity. We sequenced the genomic DNA spanning BRI1 in the cp3 and found that cp3 has a point mutation in the region encoding the 13th LRR of BRI1, resulting in a change from serine to phenylalanine (S399F). We renamed it bri1-120. We also showed that overexpression of the wild type BRI1 protein rescued the phenotype of bri1-120. Using a GFP-tagged bri1-120 construct, we detected the bri1-120 protein in the plasma membrane, and showed that the phenotypic defects in the rosette leaves of bri1-301, a kinase-inactive weak allele of BRI1, can be restored by the overexpression of the bri1-120 proteins in bri1-301. We also produced bri1-301 mutants that were wild type in appearance by performing a genetic cross between bri1-301 and bri1-120 plants.ConclusionsWe identified a new bri1 allele, bri1-120, whose mutation site has not yet been found or characterized. Our results indicated that the extracellular LRR regions before the 70-amino acid island domain of BRI1 are important for the appropriate cellular functioning of BRI1. Also, we confirmed that a successful interallelic complementation occurs between the extracellular domain mutant allele and the cytoplasmic kinase-inactive mutant allele of BRI1 in vivo.

Project description:BackgroundCell and circadian cycles control a large fraction of cell and organismal physiology by regulating large periodic transcriptional programs that encompass anywhere from 15 to 80% of the genome despite performing distinct functions. In each case, these large periodic transcriptional programs are controlled by gene regulatory networks (GRNs), and it has been shown through genetics and chromosome mapping approaches in model systems that at the core of these GRNs are small sets of genes that drive the transcript dynamics of the GRNs. However, it is unlikely that we have identified all of these core genes, even in model organisms. Moreover, large periodic transcriptional programs controlling a variety of processes certainly exist in important non-model organisms where genetic approaches to identifying networks are expensive, time-consuming, or intractable. Ideally, the core network components could be identified using data-driven approaches on the transcriptome dynamics data already available.ResultsThis study shows that a unified set of quantified dynamic features of high-throughput time series gene expression data are more prominent in the core transcriptional regulators of cell and circadian cycles than in their outputs, in multiple organism, even in the presence of external periodic stimuli. Additionally, we observe that the power to discriminate between core and non-core genes is largely insensitive to the particular choice of quantification of these features.ConclusionsThere are practical applications of the approach presented in this study for network inference, since the result is a ranking of genes that is enriched for core regulatory elements driving a periodic phenotype. In this way, the method provides a prioritization of follow-up genetic experiments. Furthermore, these findings reveal something unexpected-that there are shared dynamic features of the transcript abundance of core components of unrelated GRNs that control disparate periodic phenotypes.

Dataset Information

EMS1 and BRI1 control separate biological processes via extracellular domain diversity and intracellular domain conservation.

Publications

EMS1 and BRI1 control separate biological processes via extracellular domain diversity and intracellular domain conservation.

Similar Datasets

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