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Arabidopsis Transcription Factor MYB102 Increases Plant Susceptibility to Aphids by Substantial Activation of Ethylene Biosynthesis.

ABSTRACT: Induction of ethylene biosynthesis by aphids increases the susceptibility of several plant species to aphids. Recent studies have indicated that some MYB transcription factors regulate the phloem-based defense against aphid infestation by modulating ethylene (ET) signaling. Arabidopsis MYB102 has previously been shown to be induced by wound signaling and regulate defense response against chewing insects. However, it remains unclear whether ArabidopsisMYB102 takes part in the defense response of plants to aphids. Here, we investigated the function of MYB102 in the response of Arabidopsis to aphid infestation. ArabidopsisMYB102 was primarily expressed in vascular tissues, and its transcription was remarkably induced by green peach aphids (GPA; Myzus persicae). The results of RNA-Sequencing revealed that overexpression of MYB102 in Arabidopsis promoted ET biosynthesis by upregulation of some 1-aminocyclopropane-1-carboxylate synthase (ACS) genes, which are rate-limiting enzymes of the ET-synthetic pathway. Enhanced ET levels led to reduced Arabidopsis resistance to GPA. Furthermore, dominant suppression of MYB102 inhibited aphid-induced increase of ET levels in Arabidopsis. In agreement with a negative regulatory role for ET in aphid defense responses, the MYB102-overexpressing lines were more susceptible to GPA than wild-type (WT) plants. Overexpression of MYB102 in Arabidopsis obviously repressed aphid-induced callose deposition. Conversely, overexpression of MYB102 failed to increase aphid susceptibility in both the ET-insensitive mutants and plants treated with inhibitors of ET signaling pathways, demonstrating that the ET was critical for promoting aphid performance conferred by overexpression of MYB102. Collectively, our findings indicate that the Arabidopsis MYB102 increases host susceptibility to GPA through the ET-dependent signaling pathways.

SUBMITTER: Zhu L

PROVIDER: S-EPMC6023100 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Arabidopsis Transcription Factor MYB102 Increases Plant Susceptibility to Aphids by Substantial Activation of Ethylene Biosynthesis.

Zhu Lin L Guo Jiansheng J Ma Zhongyou Z Wang Jianfei J Zhou Cheng C

Biomolecules 20180607 2

Induction of ethylene biosynthesis by aphids increases the susceptibility of several plant species to aphids. Recent studies have indicated that some MYB transcription factors regulate the phloem-based defense against aphid infestation by modulating ethylene (ET) signaling. Arabidopsis MYB102 has previously been shown to be induced by wound signaling and regulate defense response against chewing insects. However, it remains unclear whether ArabidopsisMYB102 takes part in the ...[more]

PMID: 29880735

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Project description:BackgroundThe phytohormone ethylene controls many processes in plant development and acts as a key signaling molecule in response to biotic and abiotic stresses: it is rapidly induced by flooding, wounding, drought, and pathogen attack as well as during abscission and fruit ripening. In kiwifruit (Actinidia spp.), fruit ripening is characterized by two distinct phases: an early phase of system-1 ethylene biosynthesis characterized by absence of autocatalytic ethylene, followed by a late burst of autocatalytic (system-2) ethylene accompanied by aroma production and further ripening. Progress has been made in understanding the transcriptional regulation of kiwifruit fruit ripening but the regulation of system-1 ethylene biosynthesis remains largely unknown. The aim of this work is to better understand the transcriptional regulation of both systems of ethylene biosynthesis in contrasting kiwifruit organs: fruit and leaves.ResultsA detailed molecular study in kiwifruit (A. chinensis) revealed that ethylene biosynthesis was regulated differently between leaf and fruit after mechanical wounding. In fruit, wound ethylene biosynthesis was accompanied by transcriptional increases in 1-aminocyclopropane-1-carboxylic acid (ACC) synthase (ACS), ACC oxidase (ACO) and members of the NAC class of transcription factors (TFs). However, in kiwifruit leaves, wound-specific transcriptional increases were largely absent, despite a more rapid induction of ethylene production compared to fruit, suggesting that post-transcriptional control mechanisms in kiwifruit leaves are more important. One ACS member, AcACS1, appears to fulfil a dominant double role; controlling both fruit wound (system-1) and autocatalytic ripening (system-2) ethylene biosynthesis. In kiwifruit, transcriptional regulation of both system-1 and -2 ethylene in fruit appears to be controlled by temporal up-regulation of four NAC (NAM, ATAF1/2, CUC2) TFs (AcNAC1-4) that induce AcACS1 expression by directly binding to the AcACS1 promoter as shown using gel-shift (EMSA) and by activation of the AcACS1 promoter in planta as shown by gene activation assays combined with promoter deletion analysis.ConclusionsOur results indicate that in kiwifruit the NAC TFs AcNAC2-4 regulate both system-1 and -2 ethylene biosynthesis in fruit during wounding and ripening through control of AcACS1 expression levels but not in leaves where post-transcriptional/translational regulatory mechanisms may prevail.

Project description:Rice is an important monocotyledonous crop worldwide; it differs from the dicotyledonous plant Arabidopsis in many aspects. In Arabidopsis, ethylene and auxin act synergistically to regulate root growth and development. However, their interaction in rice is still unclear. Here, we report that the transcriptional activation of OsEIL1 on the expression of YUC8/REIN7 and indole-3-pyruvic acid (IPA)-dependent auxin biosynthesis is required for ethylene-inhibited root elongation. Using an inhibitor of YUC activity, which regulates auxin biosynthesis via the conversion of IPA to indole-3-acetic acid (IAA), we showed that ethylene-inhibited primary root elongation is dependent on YUC-based auxin biosynthesis. By screening phenotypes of seedling primary root from mutagenesis libraries following ethylene treatment, we identified a rice ethylene-insensitive mutant, rein7-1, in which YUC8/REIN7 is truncated at its C-terminus. Mutation in YUC8/REIN7 reduced auxin biosynthesis in rice, while YUC8/REIN7 overexpression enhanced ethylene sensitivity in the roots. Moreover, YUC8/REIN7 catalyzed the conversion of IPA to IAA, truncated version at C-terminal end of the YUC8/REIN7 resulted in significant reduction of enzymatic activity, indicating that YUC8/REIN7 is required for IPA-dependent auxin biosynthesis and ethylene-inhibited root elongation in rice early seedlings. Further investigations indicated that ethylene induced YUC8/REIN7 expression and promoted auxin accumulation in roots. Addition of low concentrations of IAA rescued the ethylene response in the rein7-1, strongly demonstrating that ethylene-inhibited root elongation depends on IPA-dependent auxin biosynthesis. Genetic studies revealed that YUC8/REIN7-mediated auxin biosynthesis functioned downstream of OsEIL1, which directly activated the expression of YUC8/REIN7. Thus, our findings reveal a model of interaction between ethylene and auxin in rice seedling primary root elongation, enhancing our understanding of ethylene signaling in rice.

Dataset Information

Arabidopsis Transcription Factor MYB102 Increases Plant Susceptibility to Aphids by Substantial Activation of Ethylene Biosynthesis.

Publications

<i>Arabidopsis</i> Transcription Factor MYB102 Increases Plant Susceptibility to Aphids by Substantial Activation of Ethylene Biosynthesis.

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