Genetic aspects of potato resistance to phytophthorosis

Phytophthora infestans Mont. de Bary is the main oomycete pathogen of cultivated crops in the family Solanaceae, especially potato (Solanum tuberosum). Because potato is the fourth most cultivated crop worldwide, its annual losses from late blight are tremendous. Studies of the basic mechanisms of interaction between potato and the late blight pathogen not only expand the fundamental knowledge in this area, but also open up new possibilities for regulating these interactions in order to increase resistance to the pathogen. The interaction of potato and the late blight pathogen can be considered from a genetic point of view, and it is interesting to consider both the response of the potato to the colonization process by P. infestans and the change in gene activity in late blight during plant infection. We can also investigate this process by changing the profile of secondary metabolites of the host and the pathogen. In addition to fundamental work in this area, applied work in the form of the development of new preparations for protecting potatoes is of no less importance. This review briefly describes the main stages of studies of potato resistance to late blight, starting almost from the first works. Much attention is paid to key works on changing the profile of secondary metabolites phytoalexins. A separate section is devoted to the description of both qualitative and quantitative characteristics of potato resistance to the late blight pathogen: their contribution to overall resistance, gene mapping, and regulation capabilities. Both types of traits are important for potato breeding: quantitative resistance due to R-genes is quickly overcome by the pathogen, while quantitative trait loci make it possible to create varieties with almost absolute resistance due to the pyramid of effective genes. The latest approaches in molecular biology make it possible to study translatomic profiles, which makes it possible to look at the interaction of potatoes and the late blight pathogen at a different angle. It has been shown that the process of potato colonization affects not only the activity of various genes and the profile of secondary metabolites: proteins­markers of the response to infection from potatoes have also been identified: they are pathogen-bound proteins and plastid carbonic anhydrase. On the part of P. infestans, fungal cellulose synthase proteins and haustorium-specific membrane protein were markers of infection. Thus, the review contains information on the most relevant complex studies of the genetic mechanisms of potato resistance to late blight.

1. Avrova A.O., Boevink P.C., Young V., Grenville­Briggs L.J., van West P., Birch P.R., Whisson S.C. A novel Phytophthora infestans haustorium­specific membrane protein is required for infection of potato. Cell Microbiol. 2008;10(11):2271­2284. DOI 10.1111/j.1462­5822.2008.01206.x.

2. Ballvora A., Ercolano M.R., Weiss J., Meksem K., Bormann C.A., Oberhagemann P., Salamini F., Gebhardt C. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 2002; 30(3):361­371. DOI 10.1046/j.1365­313x.2001.01292.x.

3. Bradshaw J.E., Bryan G.J., Lees A.K., McLean K., Solomon­Blackburn R.M. Mapping the R10 and R11 genes for resistance to late blight (Phytophthora infestans) present in the potato (Solanum tuberosum) R­gene differentials of Black. Theor. Appl. Genet. 2006a; 112(4):744­751. DOI 10.1007/s00122­005­0179­9.

4. Bradshaw J.E., Hackett C.A., Lowe R., McLean K., Stewart H.E., Tierney I., Vilaro M.D., Bryan G.J. Detection of a quantitative trait locus for both foliage and tuber resistance to late blight [Phytophthora infestans (Mont.) de Bary] on chromosome 4 of a dihaploid potato clone (Solanum tuberosum subsp. tuberosum). Theor. Appl. Genet. 2006b;113(5):943­951. DOI 10.1007/s00122­006­0353­8.

5. Bradshaw J.E., Pande B., Bryan G.J., Hackett C.A., McLean K., Stewart H.E., Waugh R. Interval mapping of quantitative trait loci for resistance to late blight [Phytophthora infestans (Mont.) de Bary], height and maturity in a tetraploid population of potato (Solanum tuberosum subsp. tuberosum). Genetics. 2004;168(2):983­995. DOI 10.1534/genetics.104.030056.

6. Brugmans B., Wouters D., van Os H., Hutten R., van der Linden G., Visser R.G., van Eck H.J., van der Vossen E.A. Genetic mapping and transcription analyses of resistance gene loci in potato using NBS profiling. Theor. Appl. Genet. 2008;117(8):1379­1388. DOI 10.1007/s00122­008­0871­7.

7. Chen Q., Tian Z., Jiang R., Zheng X., Xie C., Liu J. StPOTHR1, a NDR1/HIN1­like gene in Solanum tuberosum, enhances resistance against Phytophthora infestans. Biochem. Biophys. Res. Commun. 2018;496(4):1155­1161. DOI 10.1016/j.bbrc.2018.01.162.

8. Chowdappa P., Nirmal Kumar B.J., Madhura S., Mohan Kumar S.P., Myers K.L., Fry W.E., Cooke D.E.L. Severe outbreaks of late blight on potato and tomato in South India caused by recent changes in the Phytophthora infestans population. Plant Pathol. 2015;64:191­199. DOI 10.1111/ppa.12228.

9. Chung I.M., Venkidasamy B., Upadhyaya C.P., Packiaraj G., Rajakumar G., Thiruvengadam M. Alleviation of Phytophthora infestans mediated necrotic tress in the transgenic potato (Solanum tuberosum L.) with enhanced ascorbic acid accumulation. Plants (Basel). 2019;8(10):365. DOI 10.3390/plants8100365.

10. Colignon B., Dieu M., Demazy C., Delaive E., Muhovski Y., Raes M., Mauro S. Proteomic Study of SUMOylation during Solanum tuberosum–Phytophthora infestans interactions. Mol. Plant. Microbe Interact. 2017;30(11):855­865. DOI 10.1094/MPMI­05­17­0104­R.

11. Eschen­Lippold L., Landgraf R., Smolka U., Schulze S., Heilmann M., Heilmann I., Hause G., Rosahl S. Activation of defense against Phytophthora infestans in potato by down­regulation of syntaxin gene expression. New Phytol. 2012;193(4):985­996. DOI 10.1111/j.1469­8137.2011.04024.x.

12. Fry W.E., McGrath M.T., Seaman A., Zitter T.A., McLeod A., Danies G., Small I.M., Myers K., Everts K., Gevens A.J., Gugino B.K., Johnson S.B., Judelson H., Ristaino J., Roberts P., Secor G., Seebold K.J., Snover­Clift K., Wyenandt A., Grünwald N.J., Smart C.D. The 2009 late blight pandemic in the eastern United States – causes and results. Plant Dis. 2013;97(3):296­306. DOI 10.1094/PDIS­08­12­0791­FE.

13. Fu Z.Q., Guo M., Jeong B.R., Tian F., Elthon T.E., Cerny R.L., Staiger D., Alfano J.R. A type III effector ADP­ribosylates RNA­binding proteins and quells plant immunity. Nature. 2007;447(7142):284­288. DOI 10.1038/nature05737.

14. Gebhardt C., Valkonen J.P. Organization of genes controlling disease resistance in the potato genome. Annu. Rev. Phytopathol. 2001;39: 79­102. DOI 10.1146/annurev.phyto.39.1.79.

15. Grenville­Briggs L.J., Anderson V.L., Fugelstad J., Avrova A.O., Bouzenzana J., Williams A., Wawra S., Whisson S.C., Birch P.R., Bulone V., van West P. Cellulose synthesis in Phytophthora infestans is required for normal appressorium formation and successful infection of potato. Plant Cell. 2008;20(3):720­738. DOI 10.1105/tpc.107.052043.

16. Gyetvai G., Sønderkær M., Göbel U., Basekow R., Ballvora A., Imhoff M., Kersten B., Nielsen K.L., Gebhardt C. The transcriptome of compatible and incompatible interactions of potato (Solanum tuberosum) with Phytophthora infestans revealed by DeepSAGE analysis. PLoS One. 2012;7(2):e31526. DOI 10.1371/journal.pone.0031526.

17. Halim V.A., Eschen­Lippold L., Altmann S., Birschwilks M., Scheel D., Rosahl S. Salicylic acid is important for basal defense of Solanum tuberosum against Phytophthora infestans. Mol. Plant. Microbe Interact. 2007;20(11):1346­1352. DOI 10.1094/MPMI­20­11­1346.

18. Henriquez M.A., Soliman A., Li G., Hannoufa A., Ayele B.T., Daayf F. Molecular cloning, functional characterization and expression of potato (Solanum tuberosum) 1­deoxy­d­xylulose 5­phosphate synthase 1 (StDXS1) in response to Phytophthora infestans. Plant Sci. 2016;243:71­83. DOI 10.1016/j.plantsci.2015.12.001.

19. Ingram D.S. The expression of R­gene resistance to Phytophthora infestans in tissue cultures of Solanum tuberosum. J. Gen. Microbiol. 1967;49(1):99­108. DOI 10.1099/00221287­49­1­99.

20. Ingram D.S., Robertson N.F. Interaction between Phytophthora infestans and tissue cultures of Solanum tuberosum. J. Gen. Microbiol. 1965;40(3):431­437. DOI 10.1099/00221287­40­3­431.

21. Katsui N., Murai A., Takasugi M., Imaizumi K., Masamune T., Tomiyama K. The structure of rishitin, a new antifungal compound from diseased potato tubers. J. Chem. Soc. Chem. Commun. 1968;1: 43­44. DOI 10.1039/C19680000043.

22. Koch A., Biedenkopf D., Furch A., Weber L., Rossbach O., Abdellatef E., Linicus L., Johannsmeier J., Jelonek L., Goesmann A., Cardoza V., McMillan J., Mentzel T., Kogel K.H. An RNAi­based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLoS Pathog. 2016;12(10). DOI 10.1371/journal.ppat.1005901.

23. Kuć J. Phytoalexins from the Solanaceae. In: Bailey J.A., Mansfield J.W. (Eds.). Phytoalexins. Blackie; Glasgow; London, 1982; 81­105.

24. Kuć J., Rush J.S. Phytoalexins. Arch. Biochem. Biophys. 1985;236(2): 455­472. DOI 10.1016/0003­9861(85)90648­4.

25. Lim P.O., Lee I.C., Kim J., Kim H.J., Ryu J.S., Woo H.R., Nam H.G. Auxin response factor 2 (ARF2) plays a major role in regulating auxin­mediated leaf longevity. J. Exp. Bot. 2010;61(5):1419­1430. DOI 10.1093/jxb/erq010.

26. Louwes K.M., Hoekstra R., Mattheij W.M. Interspecific hybridization between the cultivated potato Solanum tuberosum subspecies tuberosum L. and the wild species S. circaeifolium subsp. circaeifolium Bitter exhibiting resistance to Phytophthora infestans (Mont.) de Bary and Globodera pallida (Stone) Behrens: 2. Sexual hybrids. Theor. Appl. Genet. 1992;84(3­4):362­370. DOI 10.1007/BF00229495.

27. Mangeon A., Junqueira R.M., Sachetto­Martins G. Functional diversity of the plant glycine­rich proteins superfamily. Plant Signal Behav. 2010;5(2):99­104. DOI 10.4161/psb.5.2.10336.

28. Mattheij W.M., Eijlander R., de Koning J.R., Louwes K.M. Interspecific hybridization between the cultivated potato Solanum tuberosum subspecies tuberosum L. and the wild species S. circaeifolium subsp. circaeifolium Bitter exhibiting resistance to Phytophthora infestans (Mont.) de Bary and Globodera pallida (Stone) Behrens: 1. Somatic hybrids. Theor. Appl. Genet. 1992;83(4):459­466. DOI 10.1007/BF00226534.

29. Mosquera T., Alvarez M.F., Jiménez­Gómez J.M., Muktar M.S., Paulo M.J., Steinemann S., Li J., Draffehn A., Hofmann A., Lübeck J., Strahwald J., Tacke E., Hofferbert H.R., Walkemeier B., Gebhardt C. Targeted and untargeted approaches unravel novel candidate genes and diagnostic SNPs for quantitative resistance of the potato (Solanum tuberosum L.) to Phytophthora infestans causing the late blight disease. PLoS One. 2016;11(6):e0156254. DOI 10.1371/journal.pone.0156254.

30. Muktar M.S., Lübeck J., Strahwald J., Gebhardt C. Selection and validation of potato candidate genes for maturity corrected resistance to Phytophthora infestans based on differential expression combined with SNP association and linkage mapping. Front Genet. 2015;6: 294. DOI 10.3389/fgene.2015.00294.

31. Müller K.O., Behr L. Mechanism of Phytophthora­resistance of potatoes. Nature. 1949;163(4143):498­499. DOI 10.1038/163498a0.

32. Odeny D.A., Stich B., Gebhardt C. Physical organization of mixed protease inhibitor gene clusters, coordinated expression and association with resistance to late blight at the StKI locus on potato chromosome III. Plant Cell Environ. 2010;33(12):2149­2161. DOI 10.1111/j.1365­3040.2010.02213.x.

33. Pajerowska­Mukhtar K., Stich B., Achenbach U., Ballvora A., Lü­ beck J., Strahwald J., Tacke E., Hofferbert H.R., Ilarionova E., Bellin D., Walkemeier B., Basekow R., Kersten B., Gebhardt C. Single nucleotide polymorphisms in the allene oxide synthase 2 gene are associated with field resistance to late blight in populations of tetraploid potato cultivars. Genetics. 2009;181(3):1115­1127. DOI 10.1534/genetics.108.094268.

34. Park C.J., Park C.B., Hong S.S., Lee H.S., Lee S.Y., Kim S.C. Characterization and cDNA cloning of two glycine­ and histidine­rich antimicrobial peptides from the roots of shepherd’s purse, Capsella bursa­pastoris. Plant Mol. Biol. 2000;44(2):187­197. DOI 10.1023/a:1006431320677.

35. Park T.H., Vleeshouwers V.G., Huigen D.J., van der Vossen E.A., van Eck H.J., Visser R.G. Characterization and high­resolution mapping of a late blight resistance locus similar to R2 in potato. Theor. Appl. Genet. 2005;111(3):591­597. DOI 10.1007/s00122­005­2050­4.

36. Poland J.A., Balint­Kurti P.J., Wisser R.J., Pratt R.C., Nelson R.J. Shades of gray: the world of quantitative disease resistance. Trends Plant Sci. 2009;14(1):21­29. DOI 10.1016/j.tplants.2008.10.006.

37. Quattrocchio F., Verweij W., Kroon A., Spelt C., Mol J., Koes R. PH4 of Petunia is an R2R3 MYB protein that activates vacuolar acidification through interactions with basic­helix­loop­helix transcription factors of the anthocyanin pathway. Plant Cell. 2006;18(5):1274­1291. DOI 10.1105/tpc.105.034041.

38. Rauscher G., Simko I., Mayton H., Bonierbale M., Smart C.D., Grünwald N.J., Greenland A., Fry W.E. Quantitative resistance to late blight from Solanum berthaultii cosegregates with R(Pi­ber): insights in stability through isolates and environment. Theor. Appl. Genet. 2010;121(8):1553­1567. DOI 10.1007/s00122­010­1410­x.

39. Restrepo S., Myers K.L., del Pozo O., Martin G.B., Hart A.L., Buell C.R., Fry W.E., Smart C.D. Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Mol. Plant Microbe Interact. 2005;18(9):913­922. DOI 10.1094/MPMI­18­0913.

40. Robertson N.F., Friend J., Aveyard M., Brown J., Huffee M., Homans A.L. The accumulation of phenolic acids in tissue culture pathogen combinations of Solanum tuberosum and Phytophthora infestans. J. Gen. Microbiol. 1968;54(2):261­268. DOI 10.1099/00221287­54­2­261.

41. Rohwer F., Fritzemeier K.H., Scheel D., Hahlbrock K. Biochemical reactions of different tissues of potato (Solanum tuberosum) to zoospores or elicitors from Phytophthora infestans: Accumulation of sesquiterpenoid phytoalexins. Planta. 1987;170(4):556­561. DOI 10.1007/BF00402991.

42. Ruocco M., Ambrosino P., Lanzuise S., Woo S.L., Lorito M., Scala F. Four potato (Solanum tuberosum) ABCG transporters and their expression in response to abiotic factors and Phytophthora infestans infection. J. Plant Physiol. 2011;168(18):2225­2233. DOI 10.1016/j.jplph.2011.07.008.

43. Santa J.D., Berdugo­Cely J., Cely­Pardo L., Soto­Suárez M., Mosquera T., Galeano M.C.H. QTL analysis reveals quantitative resistant loci for Phytophthora infestans and Tecia solanivora in tetraploid potato (Solanum tuberosum L.). PLoS One. 2018;13(7). DOI 10.1371/journal.pone.0199716.

44. Simko I. Comparative analysis of quantitative trait loci for foliage resistance to Phytophthora infestans in tuber­bearing Solanum species. Am. J. Pot. Res. 2002;79:125­132. DOI 10.1007/BF02881521.

45. Slaymaker D.H., Navarre D.A., Clark D., del Pozo O., Martin G.B., Klessig D.F. The tobacco salicylic acid­binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc. Natl. Acad. Sci. USA. 2002;99(18):11640­11645. DOI 10.1073/pnas.182427699.

46. Solomon­Blackburn R.M., Stewart H.E., Bradshaw J.E. Distinguishing major­gene from field resistance to late blight (Phytophthora infestans) of potato (Solanum tuberosum) and selecting for high levels of field resistance. Theor. Appl. Genet. 2007;115(1):141­149. DOI 10.1007/s00122­007­0550­0.

47. Stewart H.E., Bradshaw J.E., Pand B. The effect of the presence of R­genes for resistance to late blight (Phytophthora infestans) of potato (Solanum tuberosum) on the underlying level of field resistance. Plant Pathology. 2003;52(2):193­198. DOI 10.1046/j.1365­3059.2003.00811.x.

48. Tan M.Y., Hutten R.C., Celis C., Park T.H., Niks R.E., Visser R.G., van Eck H.J. The R(Pi­mcd1) locus from Solanum microdontum involved in resistance to Phytophthora infestans, causing a delay in infection, maps on potato chromosome 4 in a cluster of NBSLRR genes. Mol. Plant Microbe Interact. 2008;21(7):909­918. DOI 10.1094/MPMI­21­7­0909.

49. Tomiyama K., Takakuwa M., Takase N. The metabolic activity in healthy tissue neighbouring the infected cells in relation to resistance to Phytophthora infestans (Mont.) de By in potatoes. Phytopathol. Z. 1958;31:237­250.

50. Van der Vossen E., Sikkema A., Hekkert B., Gros J., Stevens P., Muskens M., Wouters D., Pereira A., Stiekema W., Allefs S. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad­spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 2003;36(6):867­882. DOI 10.1046/j.1365­313x.2003.01934.x.

51. Vert G., Walcher C.L., Chory J., Nemhauser J.L. Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc. Natl. Acad. Sci. USA. 2008;105(28):9829­9834. DOI 10.1073/pnas.0803996105.