A Gain-of-Function Screen Reveals Redundant ERF Transcription Factors Providing Opportunities for Resistance Breeding Toward the Vascular Fungal Pathogen <i>Verticillium longisporum</i>

Fröschel, Christian; Iven, Tim; Walper, Elisabeth; Bachmann, Vanessa; Weiste, Christoph; Dröge‐Laser, Wolfgang

doi:10.1094/mpmi-02-19-0055-r

Cited by 23 publications

(32 citation statements)

References 58 publications

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“…Very recently, Xiong et al (2020) reported that a knockdown of GhWRKY70D13 improved cotton resistance to V. dahliae going along with up‐regulation of genes involved in ET and jasmonic acid (JA) biosynthesis as well as increased ACC, JA and JA‐isoleucine levels. Also, Arabidopsis ERF TFs are induced in response to V. longisporum and their over‐expression caused a reduction of fungal DNA within the mutants, while RNAi against ERFs had the opposite effect (Fröschel et al , 2019). But also the opposite effect has been observed with Arabidopsis etr1 mutants being more resistant to V. dahliae (Pantelides et al , 2010).…”

Section: Discussionmentioning

confidence: 99%

Loss of function of CRT1a (calreticulin) reduces plant susceptibility toVerticillium longisporumin bothArabidopsis thalianaand oilseed rape (Brassica napus)

Pröbsting

Schenke

Hossain

et al. 2020

Plant Biotechnology Journal

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Brassica napus is highly susceptible towards Verticillium longisporum (Vl43) with no effective genetic resistance. It is believed that the fungus reprogrammes plant physiological processes by up-regulation of so-called susceptibility factors to establish a compatible interaction. By transcriptome analysis, we identified genes, which were activated/up-regulated in rapeseed after Vl43 infection. To test whether one of these genes is functionally involved in the infection process and loss of function would lead to decreased susceptibility, we firstly challenged KO lines of corresponding Arabidopsis orthologs with Vl43 and compared them with wild-type plants. Here, we report that the KO of AtCRT1a results in drastically reduced susceptibility of plants to Vl43. To prove crt1a mutation also decreases susceptibility in B. napus, we identified 10 mutations in a TILLING population. Three T3 mutants displayed increased resistance as compared to the wild type. To validate the results, we generated CRISPR/Cas-induced BnCRT1a mutants, challenged T2 plants with Vl43 and observed an overall reduced susceptibility in 3 out of 4 independent lines. Genotyping by allele-specific sequencing suggests a major effect of mutations in the CRT1a A-genome copy, while the C-genome copy appears to have no significant impact on plant susceptibility when challenged with Vl43. As revealed by transcript analysis, the loss of function of CRT1a results in activation of the ethylene signalling pathway, which may contribute to reduced susceptibility. Furthermore, this study demonstrates a novel strategy with great potential to improve plant disease resistance.

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Section: Discussionmentioning

confidence: 99%

Loss of function of CRT1a (calreticulin) reduces plant susceptibility toVerticillium longisporumin bothArabidopsis thalianaand oilseed rape (Brassica napus)

Pröbsting

Schenke

Hossain

et al. 2020

Plant Biotechnology Journal

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“…AtERF5, one of the closest orthologs to the VviERF6L clade, directly interacts with AtERF6 and 8 as well as SCL13 and MPK3 and 6 in unique combinations to respond differentially to Pseudomonas syringae [ 81 ], Botrytis cinera [ 77 ], Alternaria brassicicola [ 81 ] , and Meloidogyne incognita [ 82 ]. Aterf5/6 double mutants have enhanced susceptibility to V. longisporum , a fungus that induces severe wilting and plant death [ 83 ]. Another pathogen related example of a potential role in pathogen response shows decreased VviERF6L expression in response to Plasmopera viticola (downy mildew) in more susceptible vines and either an increase or no significant change in transcript abundance in more tolerant vines [ 84 , 85 ].…”

Section: Discussionmentioning

confidence: 99%

VviERF6Ls: an expanded clade in Vitis responds transcriptionally to abiotic and biotic stresses and berry development

Toups

Cochetel

Gray³

et al. 2020

BMC Genomics

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Background: VviERF6Ls are an uncharacterized gene clade in Vitis with only distant Arabidopsis orthologs. Preliminary data indicated these transcription factors may play a role in berry development and extreme abiotic stress responses. To better understand this highly duplicated, conserved clade, additional members of the clade were identified in four Vitis genotypes. A meta-data analysis was performed on publicly available microarray and RNA-Seq data (confirmed and expanded with RT-qPCR), and Vitis VviERF6L1 overexpression lines were established and characterized with phenotyping and RNA-Seq. Results: A total of 18 PN40024 VviERF6Ls were identified; additional VviERF6Ls were identified in Cabernet Sauvignon, Chardonnay, and Carménère. The amino acid sequences of VviERF6Ls were found to be highly conserved. VviERF6L transcripts were detected in numerous plant organs and were differentially expressed in response to numerous abiotic stresses including water deficit, salinity, and cold as well as biotic stresses such as red blotch virus, N. parvum, and E. necator. VviERF6Ls were differentially expressed across stages of berry development, peaking in the pre-veraison/veraison stage and retaining conserved expression patterns across different vineyards, years, and Vitis cultivars. Co-expression network analysis identified a scarecrow-like transcription factor and a calmodulin-like gene with highly similar expression profiles to the VviERF6L clade. Overexpression of VviERF6L1 in a Seyval Blanc background did not result in detectable morphological phenotypes. Genes differentially expressed in response to VviERF6L1 overexpression were associated with abiotic and biotic stress responses. Conclusions: VviERF6Ls represent a large and distinct clade of ERF transcription factors in grapevine. The high conservation of protein sequence between these 18 transcription factors may indicate these genes originate from a duplication event in Vitis. Despite high sequence similarity and similar expression patterns, VviERF6Ls demonstrate unique levels of expression supported by similar but heterogeneous promoter sequences. VviERF6L gene expression differed between Vitis species, cultivars and organs including roots, leaves and berries. These genes respond to berry development and abiotic and biotic stresses. VviERF6L1 overexpression in Vitis vinifera results in differential expression of genes related to phytohormone and immune system signaling. Further investigation of this interesting gene family is warranted.

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“…AtERF5, one of the closest orthologs to the VviERF6L clade, directly interacts with AtERF6 and 8 as well as SCL13 and MPK3 and 6 in unique combinations to respond differentially to Pseudomonas syringae [81], Botrytis cinera [77], Alternaria brassicicola [81], and Meloidogyne incognita [82]. Aterf5/6 double mutants have enhanced susceptibility to V. longisporum, a fungus that induces severe wilting and plant death [83]VviERF6L expression in response to Plasmopera viticola (downy mildew) in more susceptible vines and either an increase or no significant change in transcript abundance in more tolerant vines [84,85].…”

Section: Vvief6ls Were Differentially Expressed In Response To Bioticmentioning

confidence: 99%

VviERF6Ls: an expanded clade in Vitis responds transcriptionally to abiotic and biotic stresses and berry development

Toups

Cochetel

Gray

et al. 2020

Preprint

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Background VviERF6Ls are an uncharacterized gene clade in Vitis with only distant Arabidopsis orthologs. Preliminary data indicated these transcription factors may play a role in berry development and extreme abiotic stress responses. To better understand this highly duplicated, conserved clade, additional members of the clade were identified in four Vitis genotypes. A meta-data analysis was performed on publicly available microarray and RNA-Seq data (confirmed and expanded with RT-qPCR), and a Vitis VviERF6L1 overexpression line was established and characterized with phenotyping and RNA-Seq. Results A total of 18 PN40024 VviERF6Ls were identified; additional VviERF6Ls were identified in Cabernet Sauvignon, Chardonnay, and Carménère. The amino acid sequences of VviERF6Ls were found to be highly conserved. VviERF6L transcripts were detected in numerous plant organs and were differentially expressed in response to numerous abiotic stresses including water deficit, salinity, and cold as well as biotic stresses such as red blotch virus, N. parvum , and E. necator . VviERF6Ls were differentially expressed across stages of berry development, peaking in the pre-veraison/veraison stage, and retaining conserved expression patterns across different vineyards, years, and Vitis cultivars. Co-expression network analysis identified a scarecrow-like transcription factor and a calmodulin-like gene with highly similar expression profiles to the VviERF6L clade. Overexpression of VviERF6L1 in a Seyval Blanc background did not result in detectable morphological phenotypes. Genes differentially expressed in response to VviERF6L1 overexpression were associated with abiotic and biotic stress responses. Conclusions VviERF6Ls represent a large and distinct clade of ERF transcription factors in grapevine. The high conservation of protein sequence between these 18 transcription factors may indicate these genes originate from a duplication event in Vitis . Despite high sequence similarity and similar expression patterns, VviERF6Ls demonstrate unique levels of expression supported by similar but heterogeneous promoter sequences. VviERF6L gene expression differed between Vitis species, cultivars and organs including roots, leaves and berries. These genes respond to berry development and abiotic and biotic stresses. VviERF6L1 overexpression in Vitis vinifera results in differential expression of genes related to phytohormone and immune system signaling. Further investigation of this interesting gene family is warranted.

show abstract

A Gain-of-Function Screen Reveals Redundant ERF Transcription Factors Providing Opportunities for Resistance Breeding Toward the Vascular Fungal Pathogen Verticillium longisporum

Cited by 23 publications

References 58 publications

Loss of function of CRT1a (calreticulin) reduces plant susceptibility toVerticillium longisporumin bothArabidopsis thalianaand oilseed rape (Brassica napus)

Loss of function of CRT1a (calreticulin) reduces plant susceptibility toVerticillium longisporumin bothArabidopsis thalianaand oilseed rape (Brassica napus)

VviERF6Ls: an expanded clade in Vitis responds transcriptionally to abiotic and biotic stresses and berry development

VviERF6Ls: an expanded clade in Vitis responds transcriptionally to abiotic and biotic stresses and berry development

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