The C4 protein from the geminivirus <i>Tomato yellow leaf curl virus</i> confers drought tolerance in Arabidopsis through an ABA‐independent mechanism

Corrales-Gutierrez, Miguel; Medina-Puche, Laura; Yu, Yinhua; Wang, Liping; Ding, Xue; Luna, Ana P.; Bejarano, Eduardo R.; Castillo, Araceli G.; Lozano‐Durán, Rosa

doi:10.1111/pbi.13280

Cited by 44 publications

(53 citation statements)

References 11 publications

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“…When TYLCV-infected leaves are subjected to heat, the increase in the amounts of HSFA2 and HSFA2-dependent genes is less pronounced versus uninfected plants. It was reported recently that tomato and N. benthamiana agroinoculated with TYLCV present enhanced tolerance to drought; the C4 protein of TYLCV has been found to be involved in conferring drought tolerance through an ABA-independent manner in a still unknown mechanism (Corrales-Gutierrez et al, 2020).…”

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confidence: 99%

Interplay between abiotic (drought) and biotic (virus) stresses in tomato plants

Mishra

Shteinberg

Shkolnik

et al. 2021

Molecular Plant Pathology

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Environmental stresses affect agricultural production worldwide, leading to yield reductions of many crops. Drought and heat are the most serious abiotic stresses, especially in countries with hot climates. Drought, together with heat, usually stimulates plant pathogens such as viruses, bacteria, fungi, and insects. Interactions between the plant environment and pathogens modulate the plant defence responses (Prasch & Sonnewald, 2013), either weakening or enhancing them (Atkinson & Urwin, 2012).An increasing research body indicates that plant viruses modulate host responses to changes in their environment such as wounding, elevated salinity, high temperature, and atmospheric CO 2 . These changes are accompanied by alterations in the virus biology such as titre, virulence, and transmission efficiency (Bergès et al., 2020;van Munster et al., 2017).Abiotic stresses may affect the life cycle of viruses as well as the interactions between host susceptibility factors and viruses.Conversely, viruses can influence the plant response to abiotic stresses. For example, turnip mosaic virus (TuMV)-infected plants display an enhanced expression of defence genes, which is abolished in those plants exposed to abiotic stresses. Deactivation of defence responses leads to a higher susceptibility of plants to virus (Prasch & Sonnewald, 2013). Abiotic stress sensing through the Ca 2+

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confidence: 99%

Interplay between abiotic (drought) and biotic (virus) stresses in tomato plants

Mishra

Shteinberg

Shkolnik

et al. 2021

Molecular Plant Pathology

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“…The C4 protein has also been shown to be the pathogenicity determinant for numerous viruses in the Geminiviridae [4, 19, 20, 21]. Its function in TYLCV has received great attention in recent years using model plants, Arabidopsis and N. benthamiana in their studies [12, 14, 18, 22,]. Previously, Rojas and colleagues showed that TYLCV C4 is localized to the cell periphery, thus suggesting it may be involved in mediating virus cell-to-cell movement [23].…”

Section: Discussionmentioning

confidence: 99%

“…The targeting of BAM1 and BAM2 by TYLCV C4 has been shown to block RNAi signal spread from cell to cell [13]. In addition to two RLKs (BAM1 and BAM2) that have previously been shown to be involved in TYLCV C4 functions [12, 13, 14, 22], our transcriptome analysis also revealed the suppression of four RLK genes in the transgenic C4 tomato plants, indicating that the RLK-mediated plant defense system may have been compromised, leading to the development of a disease-like phenotype in the transgenic tomato plants. Thus, these four RLKs identified in the present study deserve further characterization on their functions in relationship to the TYLCV resistance and susceptibility in tomato plants.…”

Section: Discussionmentioning

confidence: 99%

“…There are likely multi-functional roles for the TYLCV C4 that would need to be further explored [10, 11, 12]. It has been shown that the TYLCV C4 protein interacts with the BARELY ANY MERISTEM 1 (BAM1) and suppresses the cell-to-cell movement of RNAi signals [13] and chloroplast-dependent anti-viral salicylic acid (SA) biosynthesis in Arabidopsis [14] Another study in Arabidopsis demonstrated that the TYLCV C4 protein interacted broadly with plant receptor-like kinases [15] It has been suggested that due to its interaction with CLV1, C4 inhibits the cooperative interaction between CLV1 and WUSCHEL, affecting their function in maintenance of stem cells in shoot meristems, resulting in the leaf curl-like symptoms [16].…”

Section: Introductionmentioning

confidence: 99%

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The tomato yellow leaf curl virus C4 protein alters the expression of plant developmental genes correlating to leaf upward cupping phenotype in tomato

Padmanabhan

Zheng

Shamimuzzaman

et al. 2021

Preprint

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Tomato yellow leaf curl virus (TYLCV), a monopartite begomovirus in the family Geminiviridae , is efficiently transmitted by the whitefly, Bemisia tabaci , and causes serious economic losses to tomato crops around the world. TYLCV-infected tomato plants develop distinctive symptoms of yellowing and leaf upper cupping. In recent years, excellent progress has been made in the characterization of TYLCV C4 protein function as a pathogenetic determinant in experimental plants, including Nicotiana benthamiana and Arabidopsis thaliana . However, molecular mechanism leading to disease symptom development in natural host plant tomato has yet to be characterized. The aim of the current study was to generate transgenic tomato plants expressing the TYLCV C4 gene and evaluate differential gene expression through comparative transcriptome analysis between the transgenic C4 plants and the transgenic green fluorescent protein ( Gfp) gene control plants. Transgenic tomato plants expressing the TYLCV C4 developed phenotypes, including leaf upward cupping and yellowing that are similar the disease symptom expressed on tomato plants infected with TYLCV. In a total of 241 differentially expressed genes identified in the transcriptome analysis, a series of plant development-related genes, including transcription factors, glutaredoxins, protein kinases, R-genes and microRNA target genes, were significantly altered. These results provide further evidence to support the important function of the C4 protein in begomovirus pathogenicity. These transgenic tomato plants could serve as basic genetic materials for further characterization of plant receptors that are interacting with the TYLCV C4.

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“…The suppression was mediated either by direct binding to the single-stranded microRNAs (miRNAs) and small interfering RNAs (siRNAs) [ 27 , 31 ] to block the cleavage or by interacting with plasma membrane proteins BAM1 or BAM2 to interfere with the intercellular spread of miRNAs or siRNAs [ 8 , 32 , 33 ]. C4 protein has also been reported to be involved in nucleocytoplasmic shuttling [ 34 ] and drought resistance [ 35 ]. However, it should be noted that the C4 proteins of different geminiviruses do not share equal functions [ 36 ], as C4 gene is the least conserved among geminivirus-encoded genes [ 8 ].…”

Section: Introductionmentioning

confidence: 99%

Identification of Crucial Amino Acids in Begomovirus C4 Proteins Involved in the Modulation of the Severity of Leaf Curling Symptoms

Dai

Tsai

et al. 2022

Viruses

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Begomoviruses frequently inflict upward or downward leaf curling symptoms on infected plants, leading to severe economic damages. Knowledge of the underlying mechanism controlling the leaf curling severity may facilitate the development of alternative disease management strategies. In this study, through genomic recombination between Ageratum yellow vein virus Nan-Tou strain (AYVV-NT) and Tomato leaf curl virus Tai-Chung Strain (TLCV-TC), which caused upward and downward leaf curling on Nicotiana benthamiana, respectively, it was found that the coding region of C4 protein might be involved in the determination of leaf curling directions. Sequence comparison and mutational analysis revealed that the cysteine and glycine at position 8 and 14 of AYVV-TC C4 protein, respectively, are involved in the modulation of leaf curling symptoms. Cross-protection assays further demonstrated that N. benthamiana inoculated with AYVV-carrying mutations of the aforementioned amino acids exhibited attenuated leaf curling symptoms under the challenge of wild-type AYVV-NT. Together, these findings revealed a new function of begomovirus C4 proteins involved in the modulation of leaf curling severity during symptom formation and suggested potential applications for managing viral diseases through manipulating the symptoms.

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The C4 protein from the geminivirus Tomato yellow leaf curl virus confers drought tolerance in Arabidopsis through an ABA‐independent mechanism

Cited by 44 publications

References 11 publications

Interplay between abiotic (drought) and biotic (virus) stresses in tomato plants

Interplay between abiotic (drought) and biotic (virus) stresses in tomato plants

The tomato yellow leaf curl virus C4 protein alters the expression of plant developmental genes correlating to leaf upward cupping phenotype in tomato

Identification of Crucial Amino Acids in Begomovirus C4 Proteins Involved in the Modulation of the Severity of Leaf Curling Symptoms

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