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Transcriptome analysis of an mvp mutant reveals important changes in global gene expression and a role for methyl jasmonate in vernalization and flowering in wheat.

ABSTRACT: The einkorn wheat mutant mvp-1 (maintained vegetative phase 1) has a non-flowering phenotype caused by deletions including, but not limited to, the genes CYS, PHYC, and VRN1. However, the impact of these deletions on global gene expression is still unknown. Transcriptome analysis showed that these deletions caused the upregulation of several pathogenesis-related (PR) and jasmonate-responsive genes. These results suggest that jasmonates may be involved in flowering and vernalization in wheat. To test this hypothesis, jasmonic acid (JA) and methyl jasmonate (MeJA) content in mvp and wild-type plants was measured. The content of JA was comparable in all plants, whereas the content of MeJA was higher by more than 6-fold in mvp plants. The accumulation of MeJA was also observed in vernalization-sensitive hexaploid winter wheat during cold exposure. This accumulation declined rapidly once plants were deacclimated under floral-inductive growth conditions. This suggests that MeJA may have a role in floral transition. To confirm this result, we treated vernalization-insensitive spring wheat with MeJA. The treatment delayed flowering with significant downregulation of both TaVRN1 and TaFT1 genes. These data suggest a role for MeJA in modulating vernalization and flowering time in wheat.

SUBMITTER: Diallo AO

PROVIDER: S-EPMC4036498 | biostudies-literature | 2014 Jun

REPOSITORIES: biostudies-literature

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Transcriptome analysis of an mvp mutant reveals important changes in global gene expression and a role for methyl jasmonate in vernalization and flowering in wheat.

Diallo Amadou Oury AO Agharbaoui Zahra Z Badawi Mohamed A MA Ali-Benali Mohamed Ali MA Moheb Amira A Houde Mario M Sarhan Fathey F

Journal of experimental botany 20140328 9

The einkorn wheat mutant mvp-1 (maintained vegetative phase 1) has a non-flowering phenotype caused by deletions including, but not limited to, the genes CYS, PHYC, and VRN1. However, the impact of these deletions on global gene expression is still unknown. Transcriptome analysis showed that these deletions caused the upregulation of several pathogenesis-related (PR) and jasmonate-responsive genes. These results suggest that jasmonates may be involved in flowering and vernalization in wheat. To ...[more]

PMID: 24683181

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Project description:The maintained vegetative phase (mvp) mutant has a non-flowering phenotype caused by deletions including, but not limited to, the genes CYS, PHYC and VRN1. However the impact of these deletions on flowering genes and global gene expression is still unknown. In this study, we showed that these deletions caused the up-regulation of several pathogenesis related (PR) and jasmonate responsive genes using microarray analysis. Our results raise the hypothesis that jasmonates may be involved in flowering. To confirm this hypothesis, the methyl-jasmonate (MeJA) and jasmonic acid (JA) content in mvp and wild type plants was measured. The content of JA was comparable in all plants while the content of MeJA was higher in mvp plants. Our transcriptomic and chemical analyses of the mvp mutants plants reveal that the deletion of the major vernalization gene TaVRN1 induces the up-regulation of the major biotic stress related genes and the accumulation of MeJA. In addition, our results demonstrate an important role of MeJA during vernalization and flowering in wheat. A total of 3 biological replicates (R1, R2 and R3) for each condition (wild type (control) and mvp mutant (mutant) ) were used for microarray analyses. Each biological replicate sample was obtained by pooling three wild type plants (control) or five mvp plants (mutant) from different plants harvested randomly. The different biological samples of einkorn spring wheat whole aerial part were ground in dry ice to fine powder and total RNA was extracted with trizol (Invitrogen, Burlington, ON, CA). Total RNA was cleaned using RNeasy plant mini kit (Qiagen) and integrity was determined on agarose gel and on a bioanalyser (Agilent 2100). Synthesized cDNAs were transcribed to cRNAs with the 3M-bM-^@M-^YIVT labelling kit (Santa Clara, CA, USA) and hybridized to the Affymetrix wheat genome array (Santa Clara, Ca, USA) at the McGill University and GM-CM-)nome QuM-CM-)bec Innovation Centre (Montreal, Qc, CA). The experimental design consisted of three biological replicates for each of the two conditions, 1: The einkorn wheat (Triticum monococcum L. 2n = 2x = 14, AmAm) wild type plants (control) and 2: the mvp plants (mutant). Thus, a total of 3 biological samples from each of the two conditions described above were used for hybridizations.

Project description:BackgroundVernalization, as a vital process in the life cycle of winter cereal, has important effects on floral organ formation and flowering time. Many morphological changes together with molecular changes occur during the vernalization period. Here, we used transcriptome sequencing to analyze the transcriptomic changes in wheat leaves before, during and after vernalization using the winter wheat cultivar 'Shiluan02-1'.ResultsA total of 16,370 differentially expressed genes were obtained across different vernalization periods. Gene Ontology enrichment analysis revealed that photoperiodism, photoprotection, photosynthesis, lipid transport and biosynthetic process, and chlorophyll metabolic process were closely related to vernalization. In addition, AP2/ERF, C2H2, bHLH, WRKY, MYB, MYB-related, and NAC transcription factors were significantly enriched during vernalization, and the transcription factor expression patterns suggested the intricate regulation of transcription factor modules in plant vernalization pathways. Analysis of gene expression patterns of the MADS-box transcription factor genes showed different expression patterns during vernalization phases, among which VERNALIZATION1 (VRN1) genes were found to gradually increase during vernalization periods from V0 to V35, while decline in the V42 phase, then increase after vernalization. The Tavrt-2 gene cooperated with Tavrn1 to regulate flowering induced by vernalization, and its expression level was rapidly increased by vernalization but declined in the V42 phase and then increased after vernalization. Some genes from the ICE-CBF-COR pathway were also identified, and additional analysis indicated that some key genes related to phytohormone biosynthesis and signal transduction were enriched during the vernalization period, such as gibberellic acid, ethylene, abscisic acid and jasmonic acid biosynthesis and signaling pathway genes.ConclusionsOur study provides valuable molecular information for future studies on wheat vernalization regulation and also serves as an excellent reference for future wheat breeding.

Project description:Most of the natural variation in wheat vernalization response is determined by allelic differences in the MADS-box transcription factor VERNALIZATION1 (VRN1). Extended exposures to low temperatures during the winter (vernalization) induce VRN1 expression and promote the transition of the apical meristem to the reproductive phase. In contrast to its Arabidopsis homolog (APETALA1), which is mainly expressed in the apical meristem, VRN1 is also expressed at high levels in the leaves, but its function in this tissue is not well understood. Using tetraploid wheat lines with truncation mutations in the two homoeologous copies of VRN1 (henceforth vrn1-null mutants), we demonstrate that a central role of VRN1 in the leaves is to maintain low transcript levels of the VRN2 flowering repressor after vernalization. Transcript levels of VRN2 were gradually down-regulated during vernalization in both mutant and wild-type genotypes, but were up-regulated after vernalization only in the vrn1-null mutants. The up-regulation of VRN2 delayed flowering by repressing the transcription of FT, a flowering-integrator gene that encodes a mobile protein that is transported from the leaves to the apical meristem to induce flowering. The role of VRN2 in the delayed flowering of the vrn1-null mutant was confirmed using double vrn1-vrn2-null mutants, which flowered two months earlier than the vrn1-null mutants. Both mutants produced normal flowers and seeds demonstrating that VRN1 is not essential for wheat flowering, which contradicts current flowering models. This result does not diminish the importance of VRN1 in the seasonal regulation of wheat flowering. The up-regulation of VRN1 during winter is required to maintain low transcript levels of VRN2, accelerate the induction of FT in the leaves, and regulate a timely flowering in the spring. Our results also demonstrate the existence of redundant wheat flowering genes that may provide new targets for engineering wheat varieties better adapted to changing environments.

Dataset Information

Transcriptome analysis of an mvp mutant reveals important changes in global gene expression and a role for methyl jasmonate in vernalization and flowering in wheat.

Publications

Transcriptome analysis of an mvp mutant reveals important changes in global gene expression and a role for methyl jasmonate in vernalization and flowering in wheat.

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