Silencing susceptibility genes in potato hinders primary infection with Phytophthora infestans at different stages

Kaile Sun , Danny Schipper , Evert Jacobsen , Richard G.F. Visser , Francine Govers , Klaas Bouwmeester , Yuling Bai

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhab058

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhab058 DOI: 10.1093/hr/uhab058
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Silencing susceptibility genes in potato hinders primary infection with Phytophthora infestans at different stages
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Abstract

Most potato cultivars are susceptible to late blight disease caused by the oomycete pathogen Phytophthora infestans. Here we report that the genetic loss of host susceptibility is a new source of resistance to prevent or diminish pathogen infection. Previously, we showed that RNAi-mediated silencing of the potato susceptibility (S) genes StDND1, StDMR1, and StDMR6 leads to increased late blight resistance. The mechanisms underlying this S-gene-mediated resistance have thus far not been identified. In this study, we examined the infection process of P. infestans in StDND1-, StDMR1-, and StDMR6-silenced potato lines. Microscopic analysis showed that penetration of P. infestans spores was hampered in StDND1-silenced plants. In StDMR1- and StDMR6-silenced plants, P. infestans infection was arrested at a primary infection stage by enhanced cell death responses . Histochemical staining revealed that StDMR1- and StDMR6-silenced plants display elevated ROS levels in cells at the infection sites. Resistance in StDND1-silenced plants, however, seems not to rely on a cell death response as ROS accumulation was found to be absent at most inoculated sites. Quantitative analysis of marker gene expression suggests that the increased resistance observed in StDND1- and StDMR6-silenced plants relies on an early onset of salicylic acid- and ethylene-mediated signaling pathways. Resistance mediated by silencing StDMR1 was found to be correlated with the early induction of salicylic acid-mediated signaling. These data provide evidence that different defense mechanisms are involved in late blight resistance mediated by functional impairment of different potato S-genes.

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Kaile Sun, Danny Schipper, Evert Jacobsen, Richard G.F. Visser, Francine Govers, Klaas Bouwmeester, Yuling Bai. Silencing susceptibility genes in potato hinders primary infection with Phytophthora infestans at different stages. Horticulture Research, 2022, 9 (1) : uhab058 DOI:10.1093/hr/uhab058

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References

[1]

Fry W. Phytophthora infestans: the plant (and R gene) destroyer . Mol Plant Pathol. 2008; 9: 385-402.

[2]

Elnahal ASM, Li J, Wang X et al. Identification of natural resistance mediated by recognition of Phytophthora infestans effector gene Avr3aEM in potato . Front Plant Sci. 2020; 11: 919.

[3]

Armstrong MR, Vosson J, Lim TY et al. Tracking disease resistance deployment in potato breeding by enrichment sequencing. Plant Biotechnol J. 2019; 17: 540-9.

[4]

Vossen JH, van Arkel G, Bergervoet M et al. The Solanum demissum R8 late blight resistance gene is an Sw-5 homologue that has been deployed worldwide in late blight resistant varieties . Theor Appl Genet. 2016; 129: 1785-96.

[5]

Rodewald J, Trognitz B . Solanum resistance genes against Phytophthora infestans and their corresponding avirulence genes . Mol Plant Pathol. 2013; 14: 740-757.

[6]

Vleeshouwers VG, Raffaele S, Vossen JH et al. Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol. 2011; 49: 507-31.

[7]

Du Y, Weide R, Zhao Z et al. RXLR effector diversity in Phytophthora infestans isolates determines recognition by potato resistance proteins; the case study AVR1 and R1. Stud Mycol. 2018; 89: 85-93.

[8]

Champouret N, Bouwmeester K, Rietman H et al. Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato . Mol Plant Microbe Interact. 2009; 22: 1535-45.

[9]

Zhu S, Li Y, Vossen JH et al. Functional stacking of three resistance genes against Phytophthora infestans in potato. Transgenic Res. 2012; 21: 89-99.

[10]

Rietman H, Bijsterbosch G, Cano LM et al. Qualitative and quantitative late blight resistance in the potato cultivar Sarpo Mira is determined by the perception of five distinct RXLR effectors. Mol Plant Microbe Interact. 2012; 25: 910-9.

[11]

Kuźnicki D, Meller B, Arasimowicz-Jelonek M et al. BABA-induced DNA methylome adjustment to intergenerational defense priming in potato to Phytophthora infestans . Front Plant Sci. 2019; 10: 650.

[12]

Yogendra KN, Dhokane D, Kushalappa AC et al. StWRKY8 transcription factor regulates benzylisoquinoline alkaloid pathway in potato conferring resistance to late blight . Plant Sci. 2017; 256: 208-16.

[13]

Du J, Verzaux E, Chaparro-Garcia A et al. Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nat Plants. 2015; 1: 15034.

[14]

Llorente B, Lopez MG, Carrari F et al. Downregulation of polyphenol oxidase in potato tubers redirects phenylpropanoid metabolism enhancing chlorogenate content and late blight resistance. Mol Breed. 2014; 34: 2049-63.

[15]

Sun K, Wolters AMA, Vossen JH et al. Silencing of six susceptibility genes results in potato late blight resistance. Transgenic Res. 2016; 25: 731-42.

[16]

Pessina S, Pavan S, Catalano D et al. Characterization of the MLO gene family in Rosaceae and gene expression analysis in Malus domestica . BMC Genomics. 2014; 15: 618.

[17]

Pavan S, Schiavulli A, Appiano M et al. Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus. Theor Appl Genet. 2011; 123: 1425-31.

[18]

Sun K, Wolters AMA, Loonen AEH et al. Down-regulation of Arabidopsis DND1 orthologs in potato and tomato leads to broad-spectrum resistance to late blight and powdery mildew. Transgenic Res. 2016; 25: 123-38.

[19]

Van Schie CC, Takken FL . Susceptibility genes 101: how to be a good host. Annu Rev Phytopathol. 2014; 52: 551-81.

[20]

Bai Y, Pavan S, Zheng Z et al. Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of mlo function. Mol Plant Microbe Interact. 2008; 21: 30-9.

[21]

Eschen-Lippold L, Landgraf R, Smolka U et al. Activation of defense against Phytophthora infestans in potato by down-regulation of syntaxin gene expression. New Phytol. 2012; 193: 985-96.

[22]

Su’udi M, Kim MG, Park SR et al. Arabidopsis cell death in compatible and incompatible interactions with Alternaria brassicicola . Mol Cells. 2011; 31: 593-601.

[23]

Genger RK, Jurkowski GI, McDowell JM et al. Signaling pathways that regulate the enhanced disease resistance of Arabidopsisdefense, no death” mutants . Mol Plant Microbe Interact. 2008; 21: 1285-96.

[24]

Ahn IP . Disturbance of the Ca2+/calmodulin-dependent signalling pathway is responsible for the resistance of Arabidopsis dnd1 against Pectobacterium carotovorum infection . Mol Plant Pathol. 2007; 8: 747-59.

[25]

Jurkowski GI, Smith RK Jr, Yu IC et al. Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the “defense, no death” phenotype . Mol Plant Microbe Interact. 2004; 17: 511-20.

[26]

Govrin EM, Levine A . The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea . Curr Biol. 2000; 10: 751-7.

[27]

Clough SJ, Fengler KA, Yu IC et al. The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 2000; 97: 9323-8.

[28]

Yu IC, Parker J, Bent AF . Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci USA 1998; 95: 7819-24.

[29]

Sun K, van Tuinen A, van Kan JAL et al. Silencing of DND1 in potato and tomato impedes conidial germination, attachment and hyphal growth of Botrytis cinerea . BMC Plant Biol. 2017; 17: 235.

[30]

Stuttmann J, Hubbertan HM, Rietz S et al. Perturbation of Arabidopsis amino acid metabolism causes incompatibility with the adapted biotrophic pathogen Hyaloperonospora arabidopsidis . Plant Cell. 2011; 23: 2788-803.

[31]

Van Damme M, Zeilmaker T, Elberse J et al. Downy mildew resistance in Arabidopsis by mutation of HOMOSERINE KINASE. Plant Cell. 2009; 21: 2179-89.

[32]

Brewer HC, Hawkins ND, Hammond-Kosack KE . Mutations in the Arabidopsis homoserine kinase gene DMR1 confer enhanced resistance to F. culmorum and F. graminearum . BMC Plant Biol. 2014; 14: 317.

[33]

Huibers RP, Loonen A, Gao D et al. Powdery mildew resistance in tomato by impairment of SlPMR4 and SlDMR1 . PLoS One. 2013; 8: 1-8, e67467.

[34]

Van Damme M, Huibers RP, Elberse J et al. Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew . Plant J. 2008; 54: 785-93.

[35]

Van Damme M, Andel A, Huibers RP et al. Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica . Mol Plant Microbe Interact. 2005; 18: 583-92.

[36]

Zeilmaker TL, Ludwig NR, Elberse J et al. DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis . Plant J. 2015; 81: 210-22.

[37]

Hasley JAR, Navet N, Tian M . CRISPR/Cas9-mediated mutagenesis of sweet basil candidate susceptibility gene ObDMR6 enhances downy mildew resistance. PLoS One. 2021; 16: e0253245.

[38]

Kieu NP, Lenman M, Wang ES et al. Mutations introduced in susceptibility genes through CRISPR/Cas9 genome editing confer increased late blight resistance in potatoes. Sci Rep. 2021; 11. 10.1038/s41598-021-83972-w

[39]

Low YC, Lawton MA, Rong D . Validation of barley 2OGO gene as a functional orthologue of Arabidopsis DMR6 gene in Fusarium head blight susceptibility . Sci Rep. 2020; 10. 10.1038/s41598-020-67006-5

[40]

Zhang X, Low YC, Lawton MA et al. CRISPR-editing of sweet basil (Ocimum basilicum L.) homoserine kinase gene for improved downy mildew disease resistance . Front Genome Ed. 2021; 3: 629769.

[41]

Bouwmeester K, Han M, Blanco-Portales R et al. The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in solanaceous plants . Plant Biotechnol J. 2014; 12: 10-6.

[42]

Dammann C, Rojo E, Sanchez-Serrano JJ et al. Abscisic acid and jasmonic acid activate wound-inducible genes in potato through separate, organ-specific signal transduction pathways. Plant J. 1997; 11: 773-82.

[43]

Barry CS, Fox EA, Yen H et al. Analysis of the ethylene response in the epinastic mutant of tomato. Plant Physiol. 2001; 127: 58-66.

[44]

Gamir J, Darwiche R, Vant Hof P et al. The sterol-binding activity of PATHOGENESIS-RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein. Plant J. 2017; 89: 502-9.

[45]

Bronkhorst J, Kasteel M, van Veen S et al. A slicing mechanism facilitates host entry by plant-pathogenic Phytophthora . Nat Microbiology. 2021; 6: 1000-6.

[46]

Avrova AO, Boevink PC, Young V et al. A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cell Microbiol. 2008; 10: 2271-84.

[47]

Pavan S, Jacobsen E, Visser RGF et al. Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed. 2010; 25: 1-12.

[48]

Boevink PC, Wang X, McLellan H et al. A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease. Nat Commun. 2016; 7: 10311.

[49]

Wang X, Boevink P, McLellan H et al. A host KH RNA-binding protein is a susceptibility factor targeted by an RXLR effector to promote late blight disease. Mol Plant. 2015; 8: 1385-95.

[50]

Yang L, McLellan H, Naqvi S et al. Potato NPH3/RPT2-like protein StNRL1, targeted by a Phytophthora infestans RXLR effector, is a susceptibility factor . Plant Physiol. 2016; 171: 645-57.

[51]

Peng A, Chen S, Lei T et al. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus . Plant Biotechnol J. 2017; 15: 1509-19.

[52]

Rehrig WZ, Ashrafi H, Hill T et al. CaDMR1 cosegregates with QTL Pc5.1 for resistance to Phytophthora capsici in pepper (Capsicum annuum) . Plant Genome. 2014; 7. https://doi.org/10.3835/plantgenome2014.03.0011.

[53]

de Toledo Thomazella DP, Brail Q, Dahlbeck D et al. CRISPR-Cas9 mediated mutagenesis of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. bioRxiv. 2016; 064824.

[54]

Vleeshouwers VG, van Dooijeweert W, Keizer LCP et al. A laboratory assay for Phytophthora infestans resistance in various Solanum species reflects the field situation . Eur J Plant Pathol. 1999; 105: 241-50.

[55]

Wang Y, Bouwmeester K, Van de Mortel JE et al. A novel Arabidopsis-oomycete pathosystem: differential interactions with Phytophthora capsici reveal a role for camalexin, indole glucosinolates and salicylic acid in defense . Plant Cell Environ. 2013; 36: 224-36.

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