Transcriptional Mechanism of Jasmonate Receptor COI1-Mediated Delay of Flowering Time in Arabidopsis

Zhai, Qingzhe; Zhang, Xin; Wu, Fangming; Feng, Hai-Long; Deng, Lijun; Xu, Li; Zhang, Min; Wang, Qiaomei; Li, Chuanyou

doi:10.1105/tpc.15.00619

Cited by 158 publications

(173 citation statements)

References 87 publications

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“…JA is also known to inhibit plant growth and delay flowering time (40,41). In accordance with this, the joxQ quadruple mutant was consistently smaller than wild-type plants (Fig.…”

Section: Resultssupporting

confidence: 77%

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.

144

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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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“…JA is also known to inhibit plant growth and delay flowering time (40,41). In accordance with this, the joxQ quadruple mutant was consistently smaller than wild-type plants (Fig.…”

Section: Resultssupporting

confidence: 77%

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.

144

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“…The JA signalling pathway plays important roles, not only in plant defense against herbivorous insects, but also in a wide range of developmental processes383940. To test if JA response was altered according to plant age, we first analysed the endogenous levels of JA and the bioactive JA-Ile.…”

Section: Resultsmentioning

confidence: 99%

Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance

et al. 2017

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Immunity deteriorates with age in animals but comparatively little is known about the temporal regulation of plant resistance to herbivores. The phytohormone jasmonate (JA) is a key regulator of plant insect defense. Here, we show that the JA response decays progressively in Arabidopsis. We show that this decay is regulated by the miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE9 (SPL9) group of proteins, which can interact with JA ZIM-domain (JAZ) proteins, including JAZ3. As SPL9 levels gradually increase, JAZ3 accumulates and the JA response is attenuated. We provide evidence that this pathway contributes to insect resistance in young plants. Interestingly however, despite the decay in JA response, older plants are still comparatively more resistant to both the lepidopteran generalist Helicoverpa armigera and the specialist Plutella xylostella, along with increased accumulation of glucosinolates. We propose a model whereby constitutive accumulation of defense compounds plays a role in compensating for age-related JA-response attenuation during plant maturation.

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“…Increasingly, evidence is revealing that JA-downstream TFs mediate the specificity of JA responses. Examples include: the basic helix-loop-helix (bHLH) TF family in plant defense responses and freezing tolerance (19,(39)(40)(41)(42)(43)(44); MYB TFs in stamen development, anthocyanin biosynthesis, fiber and trichome initiation (45)(46)(47); YAB TF family in anthocyanin biosynthesis (48); APETALA2 (AP2) TFs in regulation flower time (22); and WRKY TFs in senescence (49). Different JA-responsive TFs seem to be suppressed by particular JAZ proteins, suggesting that the diversity of JA responses could result from specific JAZ-TF interactions.…”

Section: Significancementioning

confidence: 99%

“…JA signaling also plays central roles in regulating other stress responses as well as several aspects of plant development (11). During flowering, JA signaling has been shown to regulate flower development and pollinator advertisement traits (20)(21)(22)(23). However, the role of JA signaling in regulating constitutive floral defenses has not been investigated.…”

mentioning

confidence: 99%

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

Wang

et al. 2017

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

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Optimal defense (OD) theory predicts that within a plant, tissues are defended in proportion to their fitness value and risk of predation. The fitness value of leaves varies greatly and leaves are protected by jasmonate (JA)-inducible defenses. Flowers are vehicles of Darwinian fitness in flowering plants and are attacked by herbivores and pathogens, but how they are defended is rarely investigated. We used Nicotiana attenuata, an ecological model plant with well-characterized herbivore interactions to characterize defense responses in flowers. Early floral stages constitutively accumulate greater amounts of two well-characterized defensive compounds, the volatile (E)-α-bergamotene and trypsin proteinase inhibitors (TPIs), which are also found in herbivore-induced leaves. Plants rendered deficient in JA biosynthesis or perception by RNA interference had significantly attenuated floral accumulations of defensive compounds known to be regulated by JA in leaves. By RNA-seq, we found a JAZ gene, NaJAZi, specifically expressed in early-stage floral tissues. Gene silencing revealed that NaJAZi functions as a flower-specific jasmonate repressor that regulates JAs, (E)-α-bergamotene, TPIs, and a defensin. Flowers silenced in NaJAZi are more resistant to tobacco budworm attack, a florivore. When the defensin was ectopically expressed in leaves, performance of Manduca sexta larvae, a folivore, decreased. NaJAZi physically interacts with a newly identified NINJA-like protein, but not the canonical NINJA. This NINJA-like recruits the corepressor TOPLESS that contributes to the suppressive function of NaJAZi on floral defenses. This study uncovers the defensive function of JA signaling in flowers, which includes components that tailor JA signaling to provide flower-specific defense

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Transcriptional Mechanism of Jasmonate Receptor COI1-Mediated Delay of Flowering Time in Arabidopsis

Cited by 158 publications

References 87 publications

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

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

Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance

Flower-specific jasmonate signaling regulates constitutive floral defenses in wild tobacco

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