Knockout of <i>SlTOM1</i> and <i>SlTOM3</i> results in differential resistance to tobamovirus in tomato

Kravchik, Michael; Shnaider, Yulia; Abebie, Bekele; Shtarkman, Meital; Kumari, Ritu; Kumar, Surender; Leibman, Diana; Spiegelman, Ziv; Gal‐On, Amit

doi:10.1111/mpp.13227

Cited by 16 publications

(22 citation statements)

References 38 publications

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“…one (AtrTOM1-L3) from the TOM3 clade. However, there is some disagreement between our phylogenetic analysis of TOM1 family members and that given byKravchik et al (2022). Variances in relationships were apparent (e.g., SlyTOM1-L4 and AtrTOM1-L1/L2/ L3).…”

contrasting

confidence: 62%

“…The influence of these TOM1 orthologues on TMV multiplication was scored at 4 dpi. The results showed that overexpression of TOM1 orthologues from S. lycopersicum (identical to SlTOM1a inKravchik et al, 2022), O. sativa, A. trichopoda, P. abies, and S. moellendorffii dramatically increased the GFP fluorescence in the inoculated leaves, whereas overexpression of CsuTOM1-L1 from C. subellipsoidea slightly increased the GFP fluorescence. However, overexpression of PpaTOM1-L1 from P. patens failed to allow GFP expression in the inoculated leaves (Figure 4a-g).…”

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confidence: 98%

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TOM1 family conservation within the plant kingdom for tobacco mosaic virus accumulation

Zhang

2023

Molecular Plant Pathology

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The susceptibility factor TOBAMOVIRUS MULTIPLICATION 1 (TOM1) is required for efficient multiplication of tobacco mosaic virus (TMV). Although some phylogenetic and functional analyses of the TOM1 family members have been conducted, a comprehensive analysis of the TOM1 homologues based on phylogeny from the most ancient to the youngest representatives within the plant kingdom, analysis of support for tobamovirus accumulation and interaction with other host and viral proteins has not been reported. In this study, using Nicotiana benthamiana and TMV as a model system, we functionally characterized the TOM1 homologues from N. benthamiana and other plant species from different plant lineages. We modified a multiplex genome editing tool and generated a sextuple mutant in which TMV multiplication was dramatically inhibited. We showed that TOM1 homologues from N. benthamiana exhibited variable capacities to support TMV multiplication. Evolutionary analysis revealed that the TOM1 family is restricted to the plant kingdom and probably originated in the Chlorophyta division, suggesting an ancient origin of the TOM1 family. We found that the TOM1 family acquired the ability to promote TMV multiplication after the divergence of moss and spikemoss. Moreover, the capacity of TOM1 orthologues from different plant species to promote TMV multiplication and the interactions between TOM1 and TOM2A and between TOM1 and TMV‐encoded replication proteins are highly conserved, suggesting a conserved nature of the TOM2A–TOM1–TMV Hel module in promoting TMV multiplication. Our study not only revealed a conserved nature of a gene module to promote tobamovirus multiplication, but also provides a valuable strategy for TMV‐resistant crop development.

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confidence: 62%

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confidence: 98%

TOM1 family conservation within the plant kingdom for tobacco mosaic virus accumulation

Zhang

2023

Molecular Plant Pathology

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“…Both the overexpression of these two genes enhanced the stomatal closure (Jung, et al 2008, Oh, et al 2011). The Solyc01g098190 (SlNHX4) and Solyc01g096740 (SlTOM) which encode sodium cation antiporter and metal chelator transporter were predicted to regulate stomatal closure and ion transmembrane transport (Ali, et al 2021, Keisham, et al 2018, Kravchik, et al 2022. And the Solyc08g066610 (SlEPFL9) encoded an epidermal patterning factor and was downregulated in PRE2OE plants.…”

Section: The Slpre2 Regulated Genes Involved In Stomatal Sizementioning

confidence: 99%

Comparative transcriptome analysis reveals the function of SlPRE2 in multiple phytohormones biosynthesis, signal transduction and stomatal development in tomato

Zhu

Luo

et al. 2023

Plant Cell Rep

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As a member of the basic/helix-loop-helix family transcription factors, the atypical bHLH Paclobutrazol Resistances (PREs) regulate plant morphology, cell size, pigment metabolism and abiotic stress in response to different phytohormones. However, little is known about the network regulation mechanisms of PREs regulated plant growth and development. In this study, the function and mechanism of SlPRE2 in tomato plant growth and development were investigated. The Quantitative RT-PCR results showed that the expression of SlPRE2 was regulated by multiple phytohormones and abiotic stresses. And it showed a light-repressed expression in photoperiod. The RNA-seq results revealed that the SlPRE2 regulated many genes involved in photosynthesis, chlorophyll metabolism, phytohormone metabolism and signaling, and carbohydrate metabolism, suggesting the role of SlPRE2 in gibberellin, brassinosteroid, auxin, cytokinin, abscisic acid and salicylic acid regulated plant development process. Moreover, the SlPRE2 overexpression plants showed widely opened stomata in young leaves, and four genes involved in stomatal development showed changed expression. Overall, the results demonstrate the regulation mechanism of SlPRE2 regulated phytohormone and stress response and the function of SlPRE2 in stomatal development in tomato. These ndings provide useful clues for understanding the molecular mechanisms of SlPRE2 regulated plant growth and development in tomato. Key MessageTranscriptome, physiology and qRT-PCR analysis revealed the potential mechanism of SlPRE2 regulated plant growth and stomatal size via multiple phytohormone pathways in tomato.

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“…The suppression of functional genes and viral proteins is also emerging as a promising alternative to confer resistance against tobamoviruses. Examples worthy of note are the works of Ishikawa et al ( 2022 ) and Kravchik et al ( 2022 ), in which sequences homologous to genes indispensable for tobamovirus replication from Arabidopsis were edited in tomato using CRISPR/Cas9 (see below). Notably, several genetic sequences with unknown functions have been proposed as potential candidates for inhibiting ToBRFV components (e.g., NBS , RLP , and RLK genes reported by Andolfo et al, 2013 ).…”

Section: Dominant Resistance (R) and Recessive Gene Repertoire Agains...mentioning

confidence: 99%

“…Using the same editing tool, Kravchik et al ( 2022 ) reported resistance to ToBRFV in S. lycopersicum cv. M82.…”

Section: Characterizing Tobrfv Proteins a Fundamental Step For Breedi...mentioning

confidence: 99%

Understanding tobamovirus-plant interactions: implications for breeding resistance to tomato brown rugose fruit virus

et al. 2022

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The genus Tobamovirus comprises a group of single-stranded RNA viruses that affect a wide variety of vegetables of economic importance. Tobamoviruses express a series of proteins that interact with the plant’s cellular machinery, allowing viral infection; during incompatible interactions, active defense is mediated by host proteins encoded by resistance genes. The genes conferring viral resistance and tolerance in non-susceptible hosts have been studied for their ability to transfer desired resistance traits to different crops. The N gene from Nicotiana spp., the repertoire of Tm genes in Solanum spp., the L locus from Capsicum spp., and TOM genes are the most studied genetic sequences for understanding resistance to tobamoviruses. Through classical plant breeding and genetic engineering techniques, it has been possible to introgress these resistance genes ( R ) into new species. However, new reports highlight the ability of tobamoviruses to overcome R -mediated defense. One of the most notorious recent cases is the tomato brown rugose fruit virus (ToBRFV). The main characteristic of ToBRFV is its capacity to overcome the resistance mediated by the Tm-2 2 gene, resulting in a limited repertoire of options to combat the virus. To defeat emerging viruses, it is necessary to apply the knowledge from other tobamoviruses-host relationships and use new technologies such as genome-wide association studies (GWAS) to understand and associate the architecture of resistance genes present in the Solanaceae family for the benefit of plant breeding. Although new genomic tools such as CRISPR systems open the possibility of coping with viral diseases, there are no commercial ToBRFV-resistant tomato varieties. Hence, the world’s leading seed suppliers compete to develop and bring these varieties to market. Supplementary Information The online version contains supplementary material available at 10.1007/s42161-022-01287-9.

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Knockout of SlTOM1 and SlTOM3 results in differential resistance to tobamovirus in tomato

Cited by 16 publications

References 38 publications

TOM1 family conservation within the plant kingdom for tobacco mosaic virus accumulation

TOM1 family conservation within the plant kingdom for tobacco mosaic virus accumulation

Comparative transcriptome analysis reveals the function of SlPRE2 in multiple phytohormones biosynthesis, signal transduction and stomatal development in tomato

Understanding tobamovirus-plant interactions: implications for breeding resistance to tomato brown rugose fruit virus

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