References

vavilov

Вавиловский журнал генетики и селекции

Vavilov Journal of Genetics and Breeding

2500-3259

Institute of Cytology and Genetics of Siberian Branch of the RAS

10.18699/VJ19.523

vavilov-2203

Research Article

СЕЛЕКЦИЯ РАСТЕНИЙ НА ИММУНИТЕТ И ПРОДУКТИВНОСТЬ

PLANT BREEDING FOR IMMUNITY AND PERFORMANCE

Разнообразие механизмов устойчивости, вовлеченных в многоуровневый иммунитет пшеницы к ржавчинным заболеваниям

Resistance mechanisms involved in complex immunity of wheat against rust diseases

https://orcid.org/0000-0001-8047-5695

Сколотнева

Е. С.

Skolotneva

E. S.

sk-ska@yandex.ru

https://orcid.org/0000-0001-8590-847X

Салина

Е. А.

Salina

E. A.

Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics, SB RASRussian Federation

2019

22082019

235542550

2019

Сколотнева Е.С., Салина Е.А.

Skolotneva E.S., Salina E.A.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://vavilov.elpub.ru/jour/article/view/2203

Обзор посвящен раскрытию современной концепции фитоиммунитета как многоуровневой системы защиты растения-хозяина, контролируемой комбинациями мажорных и минорных генов (локусов) устойчивости. Подробно разбирается модель «зигзаг» для описания молекулярных основ фитоиммунитета с ключевыми понятиями: ассоциированные с патогенами лиганды, запускающие врожденный иммунитет, дуальность эффекторов, способных вызывать восприимчивость растения, а при взаимодействии с продуктами генов устойчивости включать реакцию сверхчувствительности или альтернативные механизмы защиты. Выделено три различных типа устойчивости у злаков: 1) базовая устойчивость, обеспечиваемая рецепторными белками, локализованными в плазматической мембране; 2) расоспецифическая устойчивость, обеспечиваемая внутриклеточными R-рецепторами иммунного ответа; 3) частичная устойчивость, контролируемая локусами количественных признаков. Система «мягкая пшеница (Triticum aestivum) – возбудитель бурой ржавчины (Puccinia triticina)» является интересной моделью для наблюдения всех перечисленных механизмов устойчивости, так как стратегия данного патогена направлена на конститутивное использование ресурсов хозяина. Рассмотрены известные гены пшеницы, отвечающие за различные проявления устойчивости к бурой ржавчине: расоспецифические гены (Lr1, Lr10, Lr19, Lr21); гены возрастной устойчивости, запускающие реакцию сверхчувствительности (Lr12, Lr13, Lr22a, Lr22b, Lr35, Lr48, Lr49); и гены, реализующие альтернативные механизмы частичной устойчивости (Lr34, Lr46, Lr67, Lr77). Кроме того, недавно показано участие некоторых R-генов пшеницы в реализации прегаусториальной устойчивости к возбудителю бурой ржавчины: Lr1, Lr3a, Lr9, LrB, Lr19, Lr21, Lr38. Наличие в генотипе указанных генов позволяет останавливать ранний патогенез посредством следующих механизмов: дезориентация и ветвление ростковой гифы; формирование аберрантных структур проникновения гриба (аппрессорий, подустьичная везикула); аккумуляция каллозы в клеточных стенках мезофилла. Эффективность селекции на иммунитет повышается за счет накопления данных о разнообразных механизмах устойчивости пшеницы к ржавчинным заболеваниям, которые обобщены в данном обзоре.

The review is devoted to the disclosure of the modern concept of plant immunity as a hierarchical system of plant host protection, controlled by combinations of major and minor resistance genes (loci). The “zigzag” model is described in detail for discussing the molecular bases of plant immunity with key concepts: pathogen-associated molecular patterns triggering innate immunity, ambivalent effectors causing susceptibility, but when interacting with resistance genes, a hypersensitive reaction or alternative defense mechanisms. There are three types of resistance in cereals: (1) basal resistance provided by plasma membrane-localized receptors proteins; (2) racespecific resistance provided by intracellular immune R-receptors; (3) partial resistance conferred by quantitative gene loci. The system ‘wheat (Triticum aestivum) – the fungus causing leaf rust (Puccinia triticina)’ is an interesting model for observing all the resistance mechanisms listed above, since the strategy of this pathogen is aimed at the constitutive use of host resources. The review focuses on known wheat genes responsible for various types of resistance to leaf rust: race-specific genes Lr1, Lr10, Lr19, and Lr21; adult resistance genes which are hypersensitive Lr12, Lr13, Lr22a, Lr22b, Lr35, Lr48, and Lr49; nonhypersensitive genes conferring partial resistance Lr34, Lr46, Lr67, and Lr77. The involvement of some wheat R-genes in pre-haustorial resistance to leaf rust has been discovered recently: Lr1, Lr3a, Lr9, LrB, Lr19, Lr21, Lr38. The presence of these genes in the genotype ensures the interruption of early pathogenesis through the following mechanisms: disorientation and branching of the germ tube; formation of aberrant fungal penetration structures (appressorium, substomatal vesicle); accumulation of callose in mesophyll cell walls. Breeding for immunity is accelerated by implementation of data on various mechanisms of wheat resistance to rust diseases, which are summarized in this review.

пшеницаржавчинные инфекциирасоспецифическаячастичнаяпрегаусториальная устойчивостьгены Lrселекция на иммунитет

wheatrust diseasesrace-specificpartialpre-haustorial resistanceLr genesbreeding for immunity

This work was supported by the Russian Foundation for Basic Research, project 17-04-00507, and State Budgeted Project 02592019-0001.

References1

Вавилов Н.И. Учение об иммунитете растений к инфекционным заболеваниям (Применительно к запросам селекции). Теоретические основы селекции растений. Т. 1. М.; Л., 1935;893-900.

Vavilov N.I. The theory of plant immunity to infectious diseases. In: Theoretical Bases of Plant Breeding. Vol. 1. Moscow; Leningrad, 1935;893-900. (in Russian)

Вандерпланк Я.Е. Устойчивость растений к болезням. Пер. с англ. М.: Колос, 1972.

Van der Plank J.E. Disease Resistance in Plants. New York: Acad. Press, 1968. (Russ. ed.: Vanderplank J.E. Ustoychivost’ Rasteniy k Boleznyam. Moscow: Kolos Publ., 1972. (in Russian))

Горленко М.В. Сельскохозяйственная фитопатология. М.: Высш. шк., 1968.

Gorlenko M.B. Agricultural Plant Pathology. Moscow: Vysshaya Shkola Publ., 1968. (in Russian)

Дьяков Ю.Т. Популяционная биология фитопатогенных грибов. М.: Изд. дом «Муравей», 1998.

Diakov Yu.T. Population Biology of Phytopathogenic Fungi. Moscow: Muravey Publ., 1998. (in Russian)

Дьяков Ю.Т. На пути к общей теории иммунитета. Журн. общ. биологии. 2005;66(6):451-458.

Diakov Yu.T. Towards the general theory of immunity. Zhurnal Obshchey Biologii = Journal of General Biology. 2005;66(6):451-458. (in Russian)

Дьяков Ю.Т. Фитоиммунитет. М.: ИНФА-М, 2017.

Diakov Yu.T. Plant Disease Resistance. Moscow: INFA-M Publ., 2017. (in Russian)

Михайлова Л.А. Устойчивость пшеницы к бурой ржавчине. Идентифицированный генофонд растений и селекция. СПб.: ВИР, 2005;513-526.

Mikhaylova L.A. Genetics of wheat resistance to brown rust. In: Identified Plant Gene Pool and Breeding. St. Petersburg: VIR Publ., 2005;513-526. (in Russian)

Одинцова И.Г., Шеломова Л.Ф. Горизонтальная устойчивость: генетика и возможности преодоления паразитом. Изменчивость фитопатогенных микроорганизмов. М.: Колос, 1983;51-60.

Odintsova I.G., Shelomova L.F. Horizontal resistance: genetics and breachability by parasites. In: Variability of Pathogenic Microorganisms. Moscow: Kolos Publ., 1983;51-60. (in Russian)

Плотникова Л.Я. Участие активных форм кислорода в защите линий пшеницы с генами устойчивости рода Agropyron от бурой ржавчины. Физиология растений. 2009;56(2):200-209. DOI 10.1134/S102144370902006X

Plotnikova L.Ya. The involvement of reactive oxygen species in defense of wheat lines with the genes introgressed from Agropyron species contributing the resistance against brown rust. Russ. J. Plant Physiol. 2009;56(2):181-189. DOI 10.1134/S102144370902006X.

Пожерукова В.Е., Плотникова Л.Я., Дегтярев А.И. Устойчивость пшеницы Тимофеева к бурой ржавчине определяется генерацией активных форм кислорода и подавлением образования гаусторий гриба Puccinia triticina. Фундам. исследования. 2015; 2(2):285-292.

Pozherukova V.E., Plotnikova L.Ya., Degtyarev A.I. Timofeevi wheat resistance to leaf rust is determined by generation of reactive oxygen species and inhibition of Puccinia triticina fungus haustoria development. Fundamentalnye Issledovaniya = Fundamental Research. 2015;2(2):285-292. (in Russian)

Atienza S.G., Jafary H., Niks R.E. Accumulation of genes for susceptibility to rust fungi for which barley is nearly a nonhost results in two barley lines with extreme multiple susceptibility. Planta. 2004; 220:71-79.

Ayliffe M., Jin Y., Kang Z., Persson M., Steffenson B., Wang S., Leung H. Determining the basis of nonhost resistance in rice to cereal rusts. Euphytica. 2011;179:33-40. DOI 10.1007/s10681-010-0280-2.

Ayliffe M., Singh R., Lagudah E. Durable resistance to wheat stem rust needed. Curr. Opin. Plant Biol. 2008;11:187-192.

Bozkurt T.O., McGrann G.R.D., MacCormack R., Boyd L.A., Akkaya M.S. Cellular and transcriptional responses of wheat during compatible and incompatible race-specific interactions with Puccinia striiformis f. sp. tritici. Mol. Plant Pathol. 2010;11:625-640. DOI 10.1111/j.1364-3703.2010.00633.x.

Brueggeman R., Rostoks N., Kudrna D., Kilian A., Han F., Chen J., Druka A., Steffenson B., Kleinhofs A. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl. Acad. Sci. USA. 2002;9(14):93289333. DOI 10.1073/pnas.142284999.

Caldwell R.M. Breeding for general and specific plant disease resistance. Proc. 3rd Int. Wheat Genetic Symp. Australia. 1968;263-272. Cloutier S., McCallum B.D., Loutre C., Banks T.W., Wicker T., Feuillet C., Keller B., Jordan M.C. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol. Biol. 2007;65:93-106.

Collinge D.B., Jørgensen H.J.L., Lund O.S., Lyngkjær M.F. Engineering pathogen resistance in crop plants: current trends and future prospects. Annu. Rev. Phytopathol. 2010;48:269-291.

Cook D.E., Mesarich C.H., Thomma B.P.H.J. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopathol. 2015;53:541-563.

Dangle J.L., Jones J.D.G. Plant pathogens and integrated defense responses to infection. Nature. 2001;411:826-833.

Dodds P.N., Rathjen J.P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 2010;11:539-548.

Dyck P.L. The association of a gene for leaf rust resistance with the chromosome 7D suppressor of stem rust resistance in common wheat. Genome. 1987;29:467-469.

Ellis J.G., Lagudah E.S., Spielmeyer W., Dodds P.N. The past, present and future of breeding rust resistant wheat. Front. Plant Sci. 2014;5: 641. DOI 10.3389/fpls.2014.00641.

Feuillet C., Schachermayr G., Keller B. Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. Plant J. 1997;11(1):45-52.

Feuillet C., Travella S., Stein N., Albar L., Nublat A., Keller B. Mapbased isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc. Natl. Acad. Sci. USA. 2003;100:15253-15258.

Flor H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 1971;9:275-296.

Gennaro A., Koebner R.M.D., Ceoloni C. A candidate for Lr19, an exotic gene conditioning leaf rust resistance in wheat. Funct. Integr. Genomics. 2009;9:325-334. DOI 10.1007/s10142-009-0115-1.

Gou J.Y., Li K., Wu K., Wang X., Lin H., Cantu D., Uauy C., DobonAlonso A., Midorikawa T., Inoue K., Sánchez J., Fu D., Blechl A., Wallington E., Fahima T., Meeta M., Epstein L., Dubcovsky J. Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. Plant Cell. 2015;27:1755-1770.

Graichen F.A.S., Martinelli J.A., Federizzi L.C., Chaves M.S. Epidemiological and histological components of crown rust resistance in oat genotypes. Eur. J. Plant Pathol. 2011;131:497-510.

Hamilton E.S., Jensen G.S., Maksaev G., Katims A., Sherp A.M., Haswell E.S. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science. 2015;350(6259): 438-441. DOI 10.1126/science.aac6014.

Heath M.C. Cellular interactions between biotrophic fungal pathogens and host or nonhost plants. Can. J. Plant Pathol. 2002;24:259-264. DOI 10.1080/07060660209507007.

Herrera-Foessel S.A., Singh R.P., Lillemo M., Huerta-Espino J., Bhavani S., Singh S., Lan C., Calvo-Salazar V., Lagudah E.S. Lr67/Yr46 confers adult plant resistance to stem rust and powdery mildew in wheat. Theor. Appl. Genet. 2014;127:781-789.

Hogenhout S.A., Van der Hoorn R.A., Terauchi R., Kamoun S. Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interact. 2009;22(2):115-122. DOI 10.1094/MPMI22-2-0115.

Hu G.G., Rijkenberg F.H.J. Ultrastructural studies of the intercellular hyphae and haustorium of Puccinia recondita f. sp. tritici. J. Phytopathol. 1998;146:39-50.

Huang L., Brooks S.A., Li W., Fellers J.P., Trick H.N., Gill B.S. Mapbased cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics. 2003;164:655-664.

Huang L., Brooks S.A., Li W., Fellers J.P., Nelson J.C., Gill B.S. Evolution of new disease specificity at a simple resistance locus in a crop – weed complex: reconstitution of the Lr21 gene in wheat. Genetics. 2009:182;595-602.

Jones J.D., Dangl J.L. The plant immune system. Nature. 2006;444: 323-329. DOI 10.1038/nature05286.

Jonson R. Durable resistance: definition of, genetic control, and attainment in plant breeding. Phytopathology. 1981;71:567-568.

Kang Y.J., Kim K.H., Shim S., Yoon M.Y., Sun S., Kim M.Y., Van K., Lee S.H. Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol. 2012; 12:139.

Kolmer J.A., Su Z., Bernardo A., Bai G., Chao S. Mapping and characterization of the new adult plant leaf rust resistance gene Lr77 derived from Santa Fe winter wheat. Theor. Appl. Genet. 2018;131:15531560. DOI 10.1007/s00122-018-3097-3.

Krattinger S.G., Keller B. Molecular genetics and evolution of disease resistance in cereals. New Phytol. 2016;212:320-332.

Krattinger S.G., Lagudah E.S., Spielmeyer W., Singh R.P., Huerta-Espino J., McFadden H., Bossolini E., Selter L.L., Keller B. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360-1363.

Lagudah E.S. Molecular genetics of race non-specific rust resistance in wheat. Euphytica. 2011;179:81-91.

Lawrence G.J., Dodds P.N., Ellis J.G. Transformation of the flax rust fungus, Melampsora lini: selection via silencing of an avirulence gene. Plant J. 2010;61:364-369. DOI 10.1111/j.1365-313X.2009.04052.x.

Leonard K.J., Szabo L.J. Stem rust of small grains and grasses caused by Puccinia graminis. Mol. Plant Pathol. 2005;6:99-111.

Marone D., Russo M.A., Laidò G., Leonardis A.M., Mastrangelo A.M. Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. Int. J. Mol. Sci. 2013; 14(4):7302-7326.

McIntosh R.A., Yamazaki Y., Dubcovsky J., Rogers W.J., Morris C., Appels R., Devos K.M. Catalogue of gene symbols for wheat. KOMUGI Integrated Wheat Science Database. 2014. Available at http://www.shigen.nig.ac.jp/wheat/komugi/genes/symbolClassList.jsp

Michelmore R.W., Meyers B.C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998;8:1113-1130.

Moldenhauer J., Moerschbacher B.M., van der Westhuizen A.J. Histological investigation of stripe rust (Puccinia striiformis f. sp. tritici) development in resistant and susceptible wheat cultivars. Plant Pathol. 2006;55(4):469-474. DOI 10.1111/j.1365-3059.2006.01385.x.

Moore J.W., Herrera-Foessel S., Lan C., Schnippenkoetter W., Ayliffe M., Huerta-Espino J., Lillemo M., Viccars L., Milne R., Periyannan S., Kong X., Spielmeyer W., Talbot M., Bariana H., Patrick J.W., Dodds P., Singh R., Lagudah E. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat. Genet. 2015;47:1494-1498.

Niks R.E. Haustorium formation by Puccinia hordei in leaves of hypersensitive, partially resistant, and nonhost plant genotypes. Phytopathology. 1983;73:64-66.

Niks R.E., Marcel T.C. Nonhost and basal resistance: how to explain specificity? New Phytol. 2009;182:817-828.

Niks R.E., Qi X., Marcel T.C. Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. Annu. Rev. Phytopathol. 2015;53:445-470.

Nürnberger T., Kemmerling B. Pathogen-associated molecular patterns (PAMP) and PAMP-triggered immunity. Annu. Plant Rev. 2009;34: 16-47.

Park R.F., McIntosh R.A. Adult plant resistances to Puccinia recondite f. sp. tritici in wheat. N. Z. J. Crop Hortic. Sci. 1994;22:151-158. Parlevliet J.E., Zadoks J.C. The integrate concept disease resistance: a new view including horizontal and vertical resistance in plants. Euphytica. 1977;26:5-21.

Proietti S., Bertini L., Van der Ent S., Leon-Reyes A., Pieterse C.M.J., Tucci M., Caporale C., Caruso C. Cross activity of orthologous WRKY transcription factors in wheat and Arabidopsis. J. Exp. Bot. 2011;62(6):1975-1990. DOI 10.1093/jxb/erq396.

Schulze‐Lefert P., Panstruga R. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 2011;16:117-125.

Shang J., Tao Y., Chen X., Zou Y., Lei C., Wang J., Li X., Zhao X., Zhang M., Lu Z., Xu J., Cheng Z., Wan J., Zhu L. Identification of a new rice blast resistance gene, Pid3, by genome wide comparison of paired nucleotide-binding site leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics. 2009;182:1303-1311.

Singh R.P., Mujeeb-Kazi A., Huerta-Espino J. Lr46: a gene conferring slow-rusting resistance to leaf rust in wheat. Phytopathology. 1998; 88:890-894.

Singh R.P., Nelson J.C., Sorrells M.E. Mapping Yr28 and other genes for resistance to stripe rust in wheat. Crop Sci. 2000;40:1148-1155.

Singh R.P., Rajaram S. Resistance to Puccinia recondita f. sp. tritici in 50 Mexican bread wheat cultivars. Crop Sci. 1991;31:1472-1479.

Thomma B.P.H.J., Nurnberger T., Joosten M.H.A.J. Of PAMPs and effectors: the blurred PTI–ETI dichotomy. Plant Cell. 2011;23: 4-15.

Upadhyaya N.M., Mago R., Staskawicz B.J., Ayliffe M.A., Ellis J.G., Dodds P.N. A bacterial type III secretion assay for delivery of fungal effector proteins in to wheat. Mol. Plant Microbe Interact. 2014; 27:255-264.

van Ooijen G., Mayr G., Kasiem M.M., Albrecht M., Cornelissen B.J., Takken F.L. Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J. Exp. Bot. 2008;59(6):1383-1397.

Wang X., McCallum B.D., Fetch T., Bakkeren G., Marais G.F., Saville B.J. Comparative microscopic and molecular analysis of Thather near-isogenic lines with wheat rust resistance genes Lr2a, Lr3, LrB or Lr9 upon challenge with different Puccinia triticina races. Plant Pathol. 2013;62:698-707.

Wu H., Ni Z., Yao Y., Guo G., Sun Q. Cloning and expression profiles of 15 genes encoding WRKY transcription factors in wheat (Triticum aestivum L.). Prog. Nat. Sci. 2008;18:697-705.

Yin C., Hulbert S. Prospects for functional analysis of effectors from cereal rust fungi. Euphytica. 2011;179:57-67.

Zhang N., Wang S., Wang H., Liu D. Isolation and characterization of NBS-LRR class resistance homologous gene from wheat. Agric. Sci. China. 2011;10(8):1151-1158. DOI 10.1016/S1671-2927(11)60105-3.

The authors declare that there are no conflicts of interest present.