Hormone crosstalk in wound stress response: wound-inducible amidohydrolases can simultaneously regulate jasmonate and auxin homeostasis in<i>Arabidopsis thaliana</i>

Zhang, Tong; Poudel, Arati N.; Jewell, Jeremy B.; Kitaoka, Naoki; Staswick, Paul E.; Matsuura, Hideyuki; Koo, Abraham J.

doi:10.1093/jxb/erv521

Cited by 59 publications

(63 citation statements)

References 55 publications

(117 reference statements)

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“…Auxin conjugate hydrolases genes IAR3 which corresponds to transcripts XLOC_029902 – XLOC_048550, and ILL6 which corresponds to transcripts XLOC_010014 – XLOC_005151 (Supplementary Figure S5G), were expressed in A. thaliana and in Brassica rapa upon challenge by microorganisms (Schuller and Ludwig-Müller, 2006; Truman et al, 2010). IAR3 and ILL6 not only control auxin metabolism but are involved in deconjugation of JA-Ile which result in hormone turnover and repression of JA-responsive genes (Widemann et al, 2013; Zhang et al, 2016). This pattern also supports the involvement of these genes in JA regulation (see above).…”

Section: Resultsmentioning

confidence: 99%

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

Galindo‐González

Deyholos

2016

Front. Plant Sci.

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Fusarium oxysporum f. sp. lini is a hemibiotrophic fungus that causes wilt in flax. Along with rust, fusarium wilt has become an important factor in flax production worldwide. Resistant flax cultivars have been used to manage the disease, but the resistance varies, depending on the interactions between specific cultivars and isolates of the pathogen. This interaction has a strong molecular basis, but no genomic information is available on how the plant responds to attempted infection, to inform breeding programs on potential candidate genes to evaluate or improve resistance across cultivars. In the current study, disease progression in two flax cultivars [Crop Development Center (CDC) Bethune and Lutea], showed earlier disease symptoms and higher susceptibility in the later cultivar. Chitinase gene expression was also divergent and demonstrated and earlier molecular response in Lutea. The most resistant cultivar (CDC Bethune) was used for a full RNA-seq transcriptome study through a time course at 2, 4, 8, and 18 days post-inoculation (DPI). While over 100 genes were significantly differentially expressed at both 4 and 8 DPI, the broadest deployment of plant defense responses was evident at 18 DPI with transcripts of more than 1,000 genes responding to the treatment. These genes evidenced a reception and transduction of pathogen signals, a large transcriptional reprogramming, induction of hormone signaling, activation of pathogenesis-related genes, and changes in secondary metabolism. Among these, several key genes that consistently appear in studies of plant-pathogen interactions, had increased transcript abundance in our study, and constitute suitable candidates for resistance breeding programs. These included: an induced RPMI-induced protein kinase; transcription factors WRKY3, WRKY70, WRKY75, MYB113, and MYB108; the ethylene response factors ERF1 and ERF14; two genes involved in auxin/glucosinolate precursor synthesis (CYP79B2 and CYP79B3); the flavonoid-related enzymes chalcone synthase, dihydroflavonol reductase and multiple anthocyanidin synthases; and a peroxidase implicated in lignin formation (PRX52). Additionally, regulation of some genes indicated potential pathogen manipulation to facilitate infection; these included four disease resistance proteins that were repressed, indole acetic acid amido/amino hydrolases which were upregulated, activated expansins and glucanases, amino acid transporters and aquaporins, and finally, repression of major latex proteins.

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Section: Resultsmentioning

confidence: 99%

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

Galindo‐González

Deyholos

2016

Front. Plant Sci.

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“…Arabidopsis thaliana ecotype Col‐0 and Nicotiana benthamiana plants used in this study were grown as previously described (Zhang et al ., , ). Agro‐infectious clones of TMV‐GFP (Shivprasad et al ., ) and CMV (Fny strain) (Liao et al ., ) and were kindly provided by Prof. Xueping Zhou (Zhejiang University) and Dr. Zhouhang Gu (Zhejiang Sci‐Tech University), respectively.…”

Section: Methodsmentioning

confidence: 99%

Establishing RNA virus resistance in plants by harnessing CRISPR immune system

Zhang

Zheng

et al. 2018

Plant Biotechnology Journal

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197

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SummaryRecently, CRISPR‐Cas (clustered, regularly interspaced short palindromic repeats–CRISPR‐associated proteins) system has been used to produce plants resistant to DNA virus infections. However, there is no RNA virus control method in plants that uses CRISPR‐Cas system to target the viral genome directly. Here, we reprogrammed the CRISPR‐Cas9 system from Francisella novicida to confer molecular immunity against RNA viruses in Nicotiana benthamiana and Arabidopsis plants. Plants expressing FnCas9 and sgRNA specific for the cucumber mosaic virus (CMV) or tobacco mosaic virus (TMV) exhibited significantly attenuated virus infection symptoms and reduced viral RNA accumulation. Furthermore, in the transgenic virus‐targeting plants, the resistance was inheritable and the progenies showed significantly less virus accumulation. These data reveal that the CRISPR/Cas9 system can be used to produce plant that stable resistant to RNA viruses, thereby broadening the use of such technology for virus control in agricultural field.

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“…In 174 2ah and 3cyp lines, a significant overaccumulation of JA-Ile was recorded at 1 hpw and was 175 prolonged in 3cyp, extending data from mutants of lower order described previously (Heitz et 176 al. 2012;Widemann et al 2013;Zhang et al 2016). In the 5ko line that has both pathways 177 impaired, a huge JA-Ile accumulation was recorded that culminated between 3-6 hpw close to 178 40-50 nmol g FW -1 .…”

Section: )mentioning

confidence: 99%

Stress- and pathway-specific impacts of impaired jasmonoyl-isoleucine (JA-Ile) catabolism on defense signaling and biotic stress resistance in Arabidopsis

Marquis

Smirnova

Poirier

et al. 2019

Preprint

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20 21 Jasmonate (JA) synthesis and signaling are essential for plant defense upregulation upon 22 46 47 48 identification of jasmonoyl-isoleucine (JA-Ile) as the critical bioactive form in 2007 (Chini et 54 al. 2007; Thines et al. 2007), many derivatives of jasmonic acid (JA) were described, resulting 55 from hydroxylation, conjugation to sugars (Miersch et al. 2008), amino acids or amino 56 cyclopropane carboxylic acid, sulfation (Gidda et al. 2003), decarboxylation and many more 57 (Wasternack and Song 2017). The enzymes responsible for these modifications have not all 58 been identified and the function of these derivatives, if any, are generally unknown. The master 59 regulator jasmonoyl-(L)-isoleucine (JA-Ile) results from a specific conjugation reaction of 60 jasmonic acid (JA) by the enzyme JASMONATE RESISTANT 1 (JAR1). In the core 61 perception and signaling pathways, JA-Ile acts as a ligand promoting the assembly of the co-62 receptor CORONATINE INSENSITIVE 1 (COI1) with distinct JASMONATE ZIM-DOMAIN 63 PROTEIN (JAZ) that otherwise powerfully repress target transcription factors and responses. 64 After assembly, COI1-JAZ is recruited into the E3 ubiquitin ligase SCF COI1 that tags JAZs for 65 proteolytic degradation, and provides the basis for JA-Ile-responsive gene de-repression (Chini 66 et al. 2007; Thines et al. 2007). Several hundreds to thousands of genes are under this control, 67 and depending on developmental stage, organ, nature of stimulus, and crosstalks with other 68 hormones, a wide array of JAZ-transcription factor combinations provide specificity to the 69 system with only one major hormonal ligand (Chini et al. 2016). Distinct JA-Ile-triggered 70 networks regulate leaf defenses against different types of aggressors and are integrated by 71 separate sets of transcription factors (TF). MYC2, a bHLH type TF, integrates (together with 72 MYC3 and MYC4) simultaneous JA/abscisic acid stimuli and defines a wound/insect-specific 73 branch reflected by induction of markers such as vegetative storage protein (VSP); 74 ERF1/ORA59 TFs integrate concomitant JA/ethylene signals into a microbe-specific branch 75 probed by plant defensin PDF1.2 (Pieterse et al. 2012; Wasternack and Hause 2013). 76 77 JA signaling, like any hormonal pathway, needs to be tightly controlled in time and space, 78 particularly because defense upregulation is costly and linked to overall growth inhibition. This 79 antagonism was long thought to be merely imposed by limited resources that need to be re-80 allocated from developmental to defense sinks (Havko et al. 2016), but recent advances have 81 shown that additional hardwire connections control growth-defense tradeoffs (Campos et al. 82 2014; Guo et al. 2018). For appropriate control of JA responses, plants rely on a number of 83 negative feedback mechanisms. In addition to JAZ repressor proteins, other negative regulators 84 were identified that repress JA responses at the promoter level, including JAV (Yan et al. 2018) 85 and the JAM subclass of bHLH (Sasaki-Sekimoto ...

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Hormone crosstalk in wound stress response: wound-inducible amidohydrolases can simultaneously regulate jasmonate and auxin homeostasis inArabidopsis thaliana

Abstract: HighlightWound-inducible and ER-located amidohydrolases with overlapping substrate specificities for IAA– and JA–amino acid conjugates regulate the production and destruction of active auxin and JA signals in wounded leaves.

Cited by 59 publications

References 55 publications

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

RNA-seq Transcriptome Response of Flax (Linum usitatissimum L.) to the Pathogenic Fungus Fusarium oxysporum f. sp. lini

Establishing RNA virus resistance in plants by harnessing CRISPR immune system

Stress- and pathway-specific impacts of impaired jasmonoyl-isoleucine (JA-Ile) catabolism on defense signaling and biotic stress resistance in Arabidopsis

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