Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways

Righetti, Karima; Vu, Joseph Ly; Pelletier, Sandra; Vu, Benoît Ly; Glaab, Enrico; Lalanne, David; Pasha, Asher; Patel, Rohan; Provart, Nicholas J.; Verdier, Jérôme; Leprince, Olivier; Buitink, Julia

doi:10.1105/tpc.15.00632

Cited by 121 publications

(211 citation statements)

References 62 publications

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“…Measuring the composition of developing and mature seeds, especially in species in which maternal tissues undergo apoptosis during the final stages of desiccation, is an excellent way to understand effects of ZE on seeds (Kendall et al, 2011;He et al, 2014;Righetti et al 2015;He et al, 2016). Temperature during seed maturation has a strong effect on DOG1 transcript levels in mature seeds, and also effects CYP707A2 gene expression, GA and ABA levels (Kendall et al, 2011;Chiang et al, 2011).…”

Section: Seed Dormancy and Germination Control By The Zygotic Environmentioning

confidence: 99%

Effects of environmental variation during seed production on seed dormancy and germination

Penfield

MacGregor

2016

EXBOTJ

132

128

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Section: Seed Dormancy and Germination Control By The Zygotic Environmentioning

confidence: 99%

Effects of environmental variation during seed production on seed dormancy and germination

Penfield

MacGregor

2016

EXBOTJ

132

128

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“…The relationship between co-expression and functional correlation was first shown with Saccharomyces cerevisiae and human transcriptome data [5–8]. Subsequently, a large number of plant studies used co-expression analysis to infer gene functions [9–17]. For example, the MYB28 and MYB29 transcription factors are co-expressed with the glucosinolate pathway genes that they regulate [9].…”

Section: Introductionmentioning

confidence: 99%

Utility and Limitations of Using Gene Expression Data to Identify Functional Associations

2016

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Gene co-expression has been widely used to hypothesize gene function through guilt-by association. However, it is not clear to what degree co-expression is informative, whether it can be applied to genes involved in different biological processes, and how the type of dataset impacts inferences about gene functions. Here our goal is to assess the utility and limitations of using co-expression as a criterion to recover functional associations between genes. By determining the percentage of gene pairs in a metabolic pathway with significant expression correlation, we found that many genes in the same pathway do not have similar transcript profiles and the choice of dataset, annotation quality, gene function, expression similarity measure, and clustering approach significantly impacts the ability to recover functional associations between genes using Arabidopsis thaliana as an example. Some datasets are more informative in capturing coordinated expression profiles and larger data sets are not always better. In addition, to recover the maximum number of known pathways and identify candidate genes with similar functions, it is important to explore rather exhaustively multiple dataset combinations, similarity measures, clustering algorithms and parameters. Finally, we validated the biological relevance of co-expression cluster memberships with an independent phenomics dataset and found that genes that consistently cluster with leucine degradation genes tend to have similar leucine levels in mutants. This study provides a framework for obtaining gene functional associations by maximizing the information that can be obtained from gene expression datasets.

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“…In angiosperms, DT is acquired at the seed maturation stage, which involves a complex regulatory network (3,4) that activates a large subset of genes involved in a number of mechanisms that influence seed survival in the dry state. The set of genes required for seed DT includes genes encoding protective proteins such as late embryogenesis abundant (LEA) (5,6) and heat shock proteins (HSPs) (7), enzymes involved in scavenging reactive oxygen species (8) and the biosynthesis of protective compounds such as oligosaccharides (3,9), and antioxidants such as tocopherols and flavonoids (10,11).…”

mentioning

confidence: 99%

Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana

González-Morales

Montes

Hayano-Kanashiro

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

122

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Desiccation tolerance (DT) is a remarkable process that allows seeds in the dry state to remain viable for long periods of time that in some instances exceed 1,000 y. It has been postulated that seed DT evolved by rewiring the regulatory and signaling networks that controlled vegetative DT, which itself emerged as a crucial adaptive trait of early land plants. Understanding the networks that regulate seed desiccation tolerance in model plant systems would provide the tools to understand an evolutionary process that played a crucial role in the diversification of flowering plants. In this work, we used an integrated approach that included genomics, bioinformatics, metabolomics, and molecular genetics to identify and validate molecular networks that control the acquisition of DT in Arabidopsis seeds. Two DT-specific transcriptional subnetworks were identified related to storage of reserve compounds and cellular protection mechanisms that act downstream of the embryo development master regulators LEAFY COTYLEDON 1 and 2, FUSCA 3, and ABSCICIC ACID INSENSI-TIVE 3. Among the transcription factors identified as major nodes in the DT regulatory subnetworks, PLATZ1, PLATZ2, and AGL67 were confirmed by knockout mutants and overexpression in a desiccationintolerant mutant background to play an important role in seed DT. Additionally, we found that constitutive expression of PLATZ1 in WT plants confers partial DT in vegetative tissues.regulatory network | desiccation tolerance | drought tolerance | seed development | oligosaccharides D esiccation tolerance (DT) can be operationally defined as the ability of an organism to dry to equilibrium with moderately dry air (50 to 70% relative humidity at 20 to 30°C) and then resume normal function when rehydrated (1). DT organisms orchestrate a complex number of responses to protect cellular structures and prevent damage to proteins and nucleic acids. Early land plants evolved mechanisms to survive harsh drying environments to successfully exploit different ecosystems on land. Therefore, it has been postulated that the initial evolution of vegetative DT, in both vegetative and reproductive stages, was a crucial step required for the colonization of land by primitive plants of a fresh water origin (2).Seed DT, a trait that allows terrestrial plants to survive long periods of sparse water until favorable conditions are present for germination, is probably part of the answer to Darwin's "abominable mystery," the sudden appearance of great angiosperm diversity in the fossil record. In angiosperms, DT is acquired at the seed maturation stage, which involves a complex regulatory network (3, 4) that activates a large subset of genes involved in a number of mechanisms that influence seed survival in the dry state. The set of genes required for seed DT includes genes encoding protective proteins such as late embryogenesis abundant (LEA) (5, 6) and heat shock proteins (HSPs) (7), enzymes involved in scavenging reactive oxygen species (8) and the biosynthesis of protective compounds such as o...

show abstract

Inference of Longevity-Related Genes from a Robust Coexpression Network of Seed Maturation Identifies Regulators Linking Seed Storability to Biotic Defense-Related Pathways

Cited by 121 publications

References 62 publications

Effects of environmental variation during seed production on seed dormancy and germination

Effects of environmental variation during seed production on seed dormancy and germination

Utility and Limitations of Using Gene Expression Data to Identify Functional Associations

Regulatory network analysis reveals novel regulators of seed desiccation tolerance in Arabidopsis thaliana

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