Extreme Resistance to Viruses in Potato and Soybean

Abstract

Plant pathogens, including viruses, negatively impact global crop production. Plants have evolved complex immune responses to pathogens. These responses are often controlled by nucleotide-binding leucine-rich repeat proteins (NLRs), which recognize intracellular, pathogen-derived proteins. Genetic resistance to plant viruses is often phenotypically characterized by programmed cell death at or near the infection site; a reaction termed the hypersensitive response. Although visualization of the hypersensitive response is often used as a hallmark of resistance, the molecular mechanisms leading to the hypersensitive response and associated cell death vary. Plants with extreme resistance to viruses rarely exhibit symptoms and have little to no detectable virus replication or spread beyond the infection site. Both extreme resistance and the hypersensitive response can be activated by the same NLR genes. In many cases, genes that normally provide an extreme resistance phenotype can be stimulated to cause a hypersensitive response by experimentally increasing cellular levels of pathogen-derived elicitor protein(s). The molecular mechanisms of extreme resistance and its relationship to the hypersensitive response are largely uncharacterized. Studies on potato and soybean cultivars that are resistant to strains of Potato virus Y (PVY), Potato virus X (PVX), and Soybean mosaic virus (SMV) indicate that abscisic acid (ABA)-mediated signaling and NLR nuclear translocation are important for the extreme resistance response. Recent research also indicates that some of the same proteins are involved in both extreme resistance and the hypersensitive response. Herein, we review and synthesize published studies on extreme resistance in potato and soybean, and describe studies in additional species, including model plant species, to highlight future research avenues that may bridge the gaps in our knowledge of plant antiviral defense mechanisms.

Transcriptome and Small RNA Profiling of Potato Virus Y Infected Potato Cultivars, Including Systemically Infected Russet Burbank

“…The Payette Russet potato cultivar exhibits extreme resistance to PVY. Extreme resistance is characterized by little or no virus replication at the site of infection and a lack of visual symptoms of either infection or an immune response (i.e., hypersensitive response) [ 19 , 54 ]. There are a small number of studies describing the transcriptional responses of particular potato cultivars to specific PVY-strains, and only one that also investigates a cultivar with extreme resistance against PVY (i.e., Sante) [ 41 ] and, thus, there is little precedent for selecting sampling time point(s) that would best represent the extreme resistance response.…”

“…This response, termed effector triggered immunity (ETI), is typified by the build-up of reactive oxygen species (ROS) in infected and surrounding cells and the induction of defense related proteins (e.g., pathogenesis-related (PR) proteins). The hypersensitive response (HR) can be induced by ETI and results in programmed cell death within the infected and surrounding areas after ROS accumulation (reviewed in [ 18 , 19 ]). HR prevents or limits the spread of pathogens that require living tissue to survive and replicate.…”

“…For example, miR482 and miR2118 families in Solanaceae target conserved P-loop domains within NLR transcripts to initiate phasiRNA biogenesis, which results in reduced expression of target genes [ 36 ]. The enzymatic activity of NLRs is also regulated post-translationally (reviewed in [ 19 ]). Proteins bound to ATP recognize and bind pathogen effectors and elicit an immune response whereas ADP-bound proteins do not [ 37 ].…”

“…Resistance to PVY is usually virus strain-dependent and immune activation in plants can present various visual symptoms [ 11 , 12 , 19 , 41 , 42 ] (reviewed in [ 4 , 13 , 19 ]). Extreme resistance is defined by a lack of symptoms and little to no detectable viral replication after inoculation.…”

Genome assembly of the popular Korean soybean cultivar Hwangkeum

“…This locus is also interesting because it is located in the middle of a heterogeneous cluster ( Suh et al 2011 ) that contain members of the NLR as well as leucine-rich repeat receptor-like kinase (LRR-RLK) multigene families, of which some members have been reported to be disease resistance genes ( Song et al 1997 ; Parniske and Jones 1999 ). A strong candidate Rsv 3 gene was proposed by a comparative sequence analysis ( Redekar et al 2016 ) and was then validated by overexpression and transient silencing ( Tran et al 2018 ; Ross et al 2021 ). When the gene arrangement at this complex region spanning 1.83 Mb delimited by sequence-based markers Satt063 and GSINDEL133985 ( Lee et al 2013 ) was compared between the Hwangkeum and Williams 82 assemblies, the order and orientation of the shared genes were remarkably consistent with each other.…”