Predicting Gene Function from Uncontrolled Expression Variation among Individual Wild-Type <i>Arabidopsis</i> Plants

Bhosale, Rahul; Jewell, Jeremy B.; Hollunder, Jens; Koo, Abraham J.; Vuylsteke, Marnik; Michoel, Tom; Hilson, Pierre; Goossens, Alain; Howe, Gregg A.; Browse, John; Maere, Steven

doi:10.1105/tpc.113.112268

Cited by 52 publications

(59 citation statements)

References 45 publications

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“…Maybe less clear is the link between genes involved in defense and their expression in aerial tissues, especially since the expression compendium we used does not contain any stress conditions. However, it has been observed that subtle variations in growth conditions are difficult to control under laboratory conditions and affect gene expression (Bhosale et al, 2013). In an analysis of functional processes that showed gene expression variation in individuals grown under tightly controlled conditions, "defense"-related functions and "hormone signaling" outperformed other functional categories (Bhosale et al, 2013).…”

Section: Functional Divergence Of Homoeologs and Their Respective Coementioning

confidence: 99%

“…However, it has been observed that subtle variations in growth conditions are difficult to control under laboratory conditions and affect gene expression (Bhosale et al, 2013). In an analysis of functional processes that showed gene expression variation in individuals grown under tightly controlled conditions, "defense"-related functions and "hormone signaling" outperformed other functional categories (Bhosale et al, 2013). This finding suggests that these specific functional processes are especially difficult to control in lab Shades of blue represent the logarithm of the enrichment P value following Benjamini-Hochberg multiple testing correction of the indicated GO term in both modules.…”

Section: Functional Divergence Of Homoeologs and Their Respective Coementioning

confidence: 99%

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Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

Smet

Sabaghian

et al. 2017

Plant Cell

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Section: Functional Divergence Of Homoeologs and Their Respective Coementioning

confidence: 99%

Section: Functional Divergence Of Homoeologs and Their Respective Coementioning

confidence: 99%

Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

Smet

Sabaghian

et al. 2017

Plant Cell

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“…As genes that share a biological function tend to be coregulated, coexpression analysis through statistical correlation and clustering can infer functional associations based on the guiltby-association principle. Besides the availability of expression database resources like Genevestigator (Zimmermann et al, 2004), ATTED-II (Obayashi et al, 2007), CORNET (De Bodt et al, 2010), and GeneMANIA (Warde-Farley et al, 2010), coexpression-based gene association networks were generated for Arabidopsis thaliana with different computational sophistication (Ma et al, 2007(Ma et al, , 2014Horan et al, 2008;Bassel et al, 2011;Kourmpetis et al, 2011;Less et al, 2011;Heyndrickx and Vandepoele, 2012;Bhosale et al, 2013). Although these studies provide "functional modules" of genes operating in abiotic stress, information on their specific regulators is lacking.…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis Ensemble Reverse-Engineered Gene Regulatory Network Discloses Interconnected Transcription Factors in Oxidative Stress

et al. 2014

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The abiotic stress response in plants is complex and tightly controlled by gene regulation. We present an abiotic stress gene regulatory network of 200,014 interactions for 11,938 target genes by integrating four complementary reverse-engineering solutions through average rank aggregation on an Arabidopsis thaliana microarray expression compendium. This ensemble performed the most robustly in benchmarking and greatly expands upon the availability of interactions currently reported. Besides recovering 1182 known regulatory interactions, cis-regulatory motifs and coherent functionalities of target genes corresponded with the predicted transcription factors. We provide a valuable resource of 572 abiotic stress modules of coregulated genes with functional and regulatory information, from which we deduced functional relationships for 1966 uncharacterized genes and many regulators. Using gain-and loss-of-function mutants of seven transcription factors grown under control and salt stress conditions, we experimentally validated 141 out of 271 predictions (52% precision) for 102 selected genes and mapped 148 additional transcription factor-gene regulatory interactions (49% recall). We identified an intricate core oxidative stress regulatory network where NAC13, NAC053, ERF6, WRKY6, and NAC032 transcription factors interconnect and function in detoxification. Our work shows that ensemble reverse-engineering can generate robust biological hypotheses of gene regulation in a multicellular eukaryote that can be tested by medium-throughput experimental validation.

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“…14 and 24-26). 12-OH-JA can be formed from 12-OH-JA-Ile by cleavage of the isoleucine group by two amidohydrolases (27,28). However, an Arabidopsis double mutant that no longer produces these enzymes still accumulates 12-OH-JA, implying that other enzymes catalyze direct hydroxylation of JA to 12-OH-JA.…”

mentioning

confidence: 99%

Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

Caarls

Elberse

Awwanah

et al. 2017

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

156

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The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JAresponsive gene expression by the bioactive form JA-isoleucine have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. Because they are induced by JA we named them JASMONATE-INDUCED OXYGENASES (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae. In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in overaccumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses.jasmonic acid | 2OG oxygenases | 12-OH-JA | plant defense

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Predicting Gene Function from Uncontrolled Expression Variation among Individual Wild-Type Arabidopsis Plants

Cited by 52 publications

References 45 publications

Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana

Arabidopsis Ensemble Reverse-Engineered Gene Regulatory Network Discloses Interconnected Transcription Factors in Oxidative Stress

Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

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