Insights into the multifunctional roles of geminivirus-encoded proteins in pathogenesis

Devendran, Ragunathan; Namgial, Tsewang; Reddy, Kiran K.; Kumar, Manish; Zarreen, Fauzia; Chakraborty, Supriya

doi:10.1007/s00705-021-05338-x

Cited by 22 publications

(25 citation statements)

References 210 publications

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“…The infectivity of TYLCSbV in different plant species/varieties including some tomato cultivars grown in the region of investigation is similar to that of AYVCNV (Table 2). Begomovirus C1 and C3 proteins are known to be involved in virus replication (Hanley‐Bowdoin et al, 2013), and the C2 and C4 proteins are known as pathogenicity determinants (Devendran et al, 2022; Li et al, 2022; Matić et al, 2016; Xie et al, 2013). Thus, some or all of the C1, C2, C3, and C4 proteins may be involved in the pathogenicity, and TYLCSbV appears to have rescued pathogenicity‐determining components from AYVCNV.…”

Section: Discussionmentioning

confidence: 99%

A shift of vector specificity acquired by a begomovirus through natural homologous recombination

Fan

Zhong

Pan

et al. 2023

Molecular Plant Pathology

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Recombination is common in plant viruses such as geminiviruses, but the ecological and pathogenic consequences have been explored only in a few cases. Here, we found that a new begomovirus, tomato yellow leaf curl Shuangbai virus (TYLCSbV), probably originated from the recombination of Ageratum yellow vein China virus (AYVCNV) and tobacco curl shoot virus (TbCSV). Agrobacterium‐mediated inoculation showed that TYLCSbV and AYVCNV have similar levels of infectivity on tomato and tobacco plants. However, the two viruses exhibit contrasting specificities for vector transmission, that is, TYLCSbV was efficiently transmitted by the whitefly Bemisia tabaci Mediterranean (MED) rather than by the whitefly B. tabaci Middle East‐Asia Minor 1 (MEAM1), whereas AYVCNV was more efficiently transmitted by MEAM1. We also showed that the transmission efficiencies of TYLCSbV and AYVCNV are positively correlated with the accumulation of the viruses in whitefly whole bodies and organs/tissues. The key coat protein amino acids that determine their accumulation are between positions 147 and 256. Moreover, field surveys suggest that MED has displaced MEAM1 in some regions where TYLCSbV was collected. Viral competition assays indicated that TYLCSbV outcompeted AYVCNV when transmitted by MED, while the outcome was the opposite when transmitted by MEAM1. Our findings suggest that recombination has resulted in a shift of vector specificity that could provide TYLCSbV with a potential selective transmission advantage, and the population shift of whitefly cryptic species could have influenced virus evolution towards an extended trajectory of transmission.

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Section: Discussionmentioning

confidence: 99%

A shift of vector specificity acquired by a begomovirus through natural homologous recombination

Fan

Zhong

Pan

et al. 2023

Molecular Plant Pathology

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“…Yet, the multiple examples of monopartite Americas begomoviruses lacking V2 [27][28][29][30][31][32]60] suggest that V2 is not essential for systemic movement for all begomoviruses. It is possible that other proteins may supply the movement functions of V2 in its absence, as begomovirus proteins are highly multifunctional [13,127]. For example, a study with the TYLCV-Israel strain showed that loss-of-function V2 mutants retain the ability to establish systemic yet attenuated infection [35].…”

Section: Discussionmentioning

confidence: 99%

Phylogeographic analysis ofBegomoviruscoat and replication-associated proteins

Crespo-Bellido,

Hoyer,

Burgos-Amengual

et al. 2023

Preprint

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Begomoviruses are globally distributed plant pathogens that significantly limit crop production. These viruses are traditionally described according to phylogeographic distribution and categorized into two groups: begomoviruses from the Africa, Asia, Europe, and Oceania (AAEO) region and begomoviruses from the Americas. Monopartite begomoviruses are more common in the AAEO region while bipartite viruses predominate in the Americas, where the begomoviruses lack the V2/AV2 gene involved in inter-cellular movement and RNA silencing suppression found in AAEO begomoviruses. While these features are generally accepted as lineage-defining, the number of known species has doubled due to sequence-based discovery since 2010. To reevaluate the geographic groupings after the rapid expansion of the genus, we conducted phylogenetic analyses for begomovirus species representatives of the two longest and most conserved begomovirus proteins: the coat and replication-associated proteins. Both proteins still largely support the broad AAEO and Americas begomovirus groupings, except for sweetpotato-infecting begomoviruses that form an independent, well-supported clade for their coat protein regardless of the region they were isolated from. Our analyses do not support more fine-scaled phylogeographic groupings. Monopartite and bipartite genome organizations are broadly interchanged throughout the phylogenies and the absence of the V2/AV2 gene is highly reflective of the split between Americas and AAEO begomoviruses. We observe significant evidence of recombination within the Americas and within the AAEO region, but rarely between the regions. We speculate that increased globalization of agricultural trade, the invasion of polyphagous whitefly vector biotypes and recombination will blur begomovirus phylogeographic delineations in the future.

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“…C4 proteins (also known as AC4 proteins of bipartite geminiviruses), encoded by monopartite geminiviruses in the genus Curtovirus , Topocuvirus , Turncurtovirus , and Begomovirus , are multifunctional proteins [ 9 , 10 ]. To date, multiple C4 proteins have been reported as disease symptom determinants that can disrupt host cell development to cause symptom formation [ 11 – 14 ]. Mutational analyses of C4/AC4 proteins have shown that mutations can alleviate disease symptoms and suppress virus accumulation in infected plants [ 15 ].…”

Section: Introductionmentioning

confidence: 99%

Geminivirus C4 proteins inhibit GA signaling via prevention of NbGAI degradation, to promote viral infection and symptom development in N. benthamiana

Guo

Lang

et al. 2022

PLoS Pathog

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The phytohormone gibberellin (GA) is a vital plant signaling molecule that regulates plant growth and defense against abiotic and biotic stresses. To date, the molecular mechanism of the plant responses to viral infection mediated by GA is still undetermined. DELLA is a repressor of GA signaling and is recognized by the F-box protein, a component of the SCFSLY1/GID2 complex. The recognized DELLA is degraded by the ubiquitin-26S proteasome, leading to the activation of GA signaling. Here, we report that ageratum leaf curl Sichuan virus (ALCScV)-infected N. benthamiana plants showed dwarfing symptoms and abnormal flower development. The infection by ALCScV significantly altered the expression of GA pathway-related genes and decreased the content of endogenous GA in N. benthamiana. Furthermore, ALCScV-encoded C4 protein interacts with the DELLA protein NbGAI and interferes with the interaction between NbGAI and NbGID2 to prevent the degradation of NbGAI, leading to inhibition of the GA signaling pathway. Silencing of NbGAI or exogenous GA3 treatment significantly reduces viral accumulation and disease symptoms in N. benthamiana plants. The same results were obtained from experiments with the C4 protein encoded by tobacco curly shoot virus (TbCSV). Therefore, we propose a novel mechanism by which geminivirus C4 proteins control viral infection and disease symptom development by interfering with the GA signaling pathway.

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Insights into the multifunctional roles of geminivirus-encoded proteins in pathogenesis

Cited by 22 publications

References 210 publications

A shift of vector specificity acquired by a begomovirus through natural homologous recombination

A shift of vector specificity acquired by a begomovirus through natural homologous recombination

Phylogeographic analysis ofBegomoviruscoat and replication-associated proteins

Geminivirus C4 proteins inhibit GA signaling via prevention of NbGAI degradation, to promote viral infection and symptom development in N. benthamiana

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