WHEAT STRIPE RUST AND INTEGRATION OF SUSTAINABLE CONTROL STRATEGIES IN CHINA

Highlights

• Stripe rust caused substantial yield losses in China.

• P. striiformis is highly variable and the change from avirulence to virulence.

• Different comprehensive control strategies were adopted in different epidemic region.

Abstract

Stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici occurs in almost all wheat-producing regions of the world. Severe countrywide epidemics in China have caused substantial yield losses. Growing resistant cultivars is the best strategy to control this disease but the pathogen can overcome resistance in wheat cultivars. The high variation in the virulence of the pathogen combined with the large areas of susceptible wheat cultivars enables the pathogen population to increase rapidly and disperse over long distances under favorable environmental conditions, resulting in severe pandemics within cropping seasons. Current stripe rust control measures are based on many years of research including the underlying epidemiology regarding year-to-year survival of the pathogen, pathways of pathogen dispersal within seasons and years, the role of P. striiformis sexual hybridization, the use of resistance sources in breeding programs, and year-round surveillance of national wheat crops that are present in different parts of the country throughout the year. All these strategies depend on accurate prediction of epidemics, more precise use of fungicides to meet national requirements and better deployment of resistance genes. New ideas with potential application in sustainable protection of stripe rust include negative regulatory gene editing, resistance gene overexpression and biological control based on microbiomes.

Graphical abstract

Keywords

sustainable disease control / integrated control Puccinia striiformis / Triticum aestivum

References

[1] Chen X M, Kang Z S, eds. Stripe Rust. Dordrect, the Netherlands: Springer Science,2017

[2] Stubbs R W. Stripe rust. In: Roelfs A P, Bushnell W R, eds. The Cereal Rusts, Vol II. New York: Academic Press, 1985, 61–101

[3] Li Z Q, Zeng S M. Wheat rusts in China. Beijing: China Agriculture Press,2002 (in Chinese)

[4] Kang Z S, Zhao J, Han D J, Zhang H C, Wang X J, Wang C F, Han Q M, Guo J, Huang L L. Status of wheat rust research and control in China. In: Proceedings of the BGRI 2010 Technical Workshop Oral Presentations. St. Petersburg, Russia, 2010, 50

[5] Boller T, He S Y. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 2009, 324(5928): 742–744

[6] Li Z. Primary discussion on breakdown of resistance of wheat cultivars to stripe rust. Journal of Northwest A&F University (Natural Science Edition), 1980, 3: 83–92 (in Chinese)

[7] Chen W Q, Kang Z S, Ma Z H, Xu S C, Jin S L, Jiang Y Y. Integrated Management of Wheat Stripe Rust Caused by Puccinia striiformis f. sp. tritici in China. Scientia Agricultura Sinica, 2013, 46(20): 4254–4262 (in Chinese)

[8] Jin Y, Szabo L J, Carson M. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology, 2010, 100(5): 432–435

[9] Zhao J, Zheng D, Zuo S X, Wang L, Huang L L, Kang Z S. Research advances in alternate host and sexual reproduction of wheat yellow rust pathogen Puccinia striiformis f. sp. tritici Erikss. et Henn. Acta Phytophylacica Sinica, 2018, 45(1): 7–19 (in Chinese)

[10] Zhao J, Wang L, Wang Z, Chen X, Zhang H, Yao J, Zhan G, Chen W, Huang L, Kang Z. Identification of eighteen Berberis species as alternate hosts of Puccinia striiformis f. sp. tritici and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology, 2013, 103(9): 927–934

[11] Wang Z, Zhao J, Chen X, Peng Y, Ji J, Zhao S, Lv Y, Huang L, Kang Z. Virulence variations of Puccinia striiformis f. sp. tritici isolates collected from Berberis spp. in China. Plant Disease, 2016, 100(1): 131–138

[12] Liu Y, Chen X Y, Ma Y, Meng Z Y, Wang F L, Yang X J, Chen X F, Li X M, Kang Z S, Zhao J. Evidence of roles of susceptible barberry in providing (primary) inocula to trigger stripe rust infection on wheat in Longnan, Gansu. Acta Phytopathologica Sinica, 2020 (in Chinese)

[13] Lu N H, Wang J F, Chen X M, Zhan G M, Chen C Q, Huang L L, Kang Z S. Spatial genetic diversity and interregional spread of Puccinia striiformis f. sp. tritici in the Northwest China. European Journal of Plant Pathology, 2011, 131(4): 685–693

[14] Wan Q, Liang J, Luo Y, Ma Z. Population genetic structure of Puccinia striiformis f. sp. tritici in northwestern China. Plant Disease, 2015, 99(12): 1764–1774

[15] Liang J, Liu X, Li Y, Wan Q, Ma Z, Luo Y. Population genetic structure and the migration of Puccinia striiformis f. sp tritici between the Gansu and Sichuan basin populations of china. Phytopathology, 2016, 106(2): 192–201

[16] Zhan G, Wang F, Wan C, Han Q, Huang L, Kang Z, Chen X. Virulence and molecular diversity of the Puccinia striiformis f. sp. tritici population in Xinjiang in relation to other regions of western China. Plant Disease, 2016, 100(1): 99–107

[17] Ministry of Agriculture and Rural Affairs of the People’s Republic of China (MARAPR). Zero growth in the use of chemical fertilisers and pesticides by 2020. Available on MARAPR website on October 11, 2020http://www.moa.gov.cn/nybgb/2015/san/201711/t20171129_5923401.htm

[18] Oliver R P. A reassessment of the risk of rust fungi developing resistance to fungicides. Pest Management Science, 2014, 70(11): 1641–1645

[19] Cook N M, Chng S, Woodman T L, Warren R, Oliver R P, Saunders D G. High frequency of fungicide resistance-associated mutations in the wheat yellow rust pathogen Puccinia striiformis f. sp. tritici. Pest Management Science, 2021, 77(7): 3358–3371

[20] International Wheat Genome Sequencing Consortium(IWGSC); Appels R, Eversole K, Stein N, Feuillet C, Keller B, Rogers J, Pozniak C J, Choulet F, Distelfeld A, Poland J, Ronen G, Sharpe A G, Barad O, Baruch K, Keeble-Gagnère G, Mascher M, Ben-Zvi G, Josselin A A, Himmelbach A, Balfourier F, Gutierrez-Gonzalez J, Hayden M, Koh C S, Muehlbauer G, Pasam R K, Paux E, Rigault P, Tibbits J, Tiwari V, Spannagl M, Lang D, Gundlach H, Haberer G, Mayer K F X, Ormanbekova D, Prade V, Šimková H, Wicker T, Swarbreck D, Rimbert H, Felder M, Guilhot N, Kaithakottil G, Keilwagen J, Leroy P, Lux T, Twardziok S, Venturini L, Juhász A, Abrouk M, Fischer I, Uauy C, Borrill P, Ramirez-Gonzalez R H, Arnaud D, Chalabi S, Chalhoub B, Cory A, Datla R, Davey M W, Jacobs J, Robinson S J, Steuernagel B, van Ex F, Wulff B B H, Benhamed M, Bendahmane A, Concia L, Latrasse D, Bartoš J, Bellec A, Berges H, Doležel J, Frenkel Z, Gill B, Korol A, Letellier T, Olsen O A, Singh K, Valárik M, van der Vossen E, Vautrin S, Weining S, Fahima T, Glikson V, Raats D, Číhalíková J, Toegelová H, Vrána J, Sourdille P, Darrier B, Barabaschi D, Cattivelli L, Hernandez P, Galvez S, Budak H, Jones J D G, Witek K, Yu G, Small I, Melonek J, Zhou R, Belova T, Kanyuka K, King R, Nilsen K, Walkowiak S, Cuthbert R, Knox R, Wiebe K, Xiang D, Rohde A, Golds T, Čížková J, Akpinar B A, Biyiklioglu S, Gao L, N’Daiye A, Kubaláková M, Šafář J, Alfama F, Adam-Blondon A F, Flores R, Guerche C, Loaec M, Quesneville H, Condie J, Ens J, Maclachlan R, Tan Y, Alberti A, Aury J M, Barbe V, Couloux A, Cruaud C, Labadie K, Mangenot S, Wincker P, Kaur G, Luo M, Sehgal S, Chhuneja P, Gupta O P, Jindal S, Kaur P, Malik P, Sharma P, Yadav B, Singh N K, Khurana J P, Chaudhary C, Khurana P, Kumar V, Mahato A, Mathur S, Sevanthi A, Sharma N, Tomar R S, Holušová K, Plíhal O, Clark M D, Heavens D, Kettleborough G, Wright J, Balcárková B, Hu Y, Salina E, Ravin N, Skryabin K, Beletsky A, Kadnikov V, Mardanov A, Nesterov M, Rakitin A, Sergeeva E, Handa H, Kanamori H, Katagiri S, Kobayashi F, Nasuda S, Tanaka T, Wu J, Cattonaro F, Jiumeng M, Kugler K, Pfeifer M, Sandve S, Xun X, Zhan B, Batley J, Bayer P E, Edwards D, Hayashi S, Tulpová Z, Visendi P, Cui L, Du X, Feng K, Nie X, Tong W, Wang L. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 2018, 361(6403): eaar7191

[21] Shewry P R. Wheat. Journal of Experimental Botany, 2009, 60(6): 1537–1553

[22] National Bureau of Statistics (NBS). Output and planting area of main crop products. Beijing: NBS, 2020. Available at NBS website on November 2, 2020

[23] National Bureau of Statistics (NBS). Import quantity of main goods. Beijing: NBS, 2020. Available at NBS website on November 2, 2020

[24] National Agro-Technical Extension and Service Centre. Prediction of occurrence trend of crop diseases and insect pests in 2021. Available at sina website on November 2, 2020 (in Chinese)

[25] Roelfs A P, Singh R P, Saari E E. Rust diseases of wheat: concepts and methods of disease management. Mexico: Cimmyt,1992

[26] Li Z Q, Shang H S. Wheat Rusts and Its Control. Shanghai: Shanghai Scientific & Technical Publishers, 1989

[27] Zadoks J C. Yellow rust on wheat studies in epidemiology and physiologic specialization. Tijdschrift Over Plantenziekten, 1961, 67(3): 69–256

[28] Rapilly F. Yellow rust epidemiology. Annual Review of Phytopathology, 1979, 17(1): 59–73

[29] Wellings C R. Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006. Australian Journal of Agricultural Research, 2007, 58(6): 567–575

[30] Sharma-Poudyal D, Chen X M, Wan A M, Zhan G M, Kang Z S, Cao S Q, Jin S L, Morgounov A, Akin B, Mert Z, Shah S J A, Bux H, Ashraf M, Sharma R C, Madariaga R, Puri K D, Wellings C, Xi K Q, Wanyera R, Manninger K, Ganzález M I, Koyda M, Sanin S, Patzek L J. Virulence Characterization of International Collections of the Wheat Stripe Rust Pathogen, Puccinia striiformis f. sp. tritici. Plant Disease, 2013, 97(3): 379–386

[31] Eriksson J, Henning E J. Die getreideroste, ihre geschichte und natur sowie massregeln genen dieselben: Bericht über die am experimentalfelde der Kgl. schwedischen landbau-akademie in den jahren 1890–93 mit staatsunten stützung ausgeführte untersuchung. Germany: Nabu Press, 1896 (in German)

[32] Straib W. Untersuchungen über das Vorkommen physiologischer Rassen des Gelbrostes (Puccinia glumarum) in den Jahren 1935/36 und über die Aggressivität einiger neuer Formen auf Getreide und Gräsern. Arb Biol Reichsanst, 1937, 22: 91–119 (in German)

[33] Hart H, Becker H.Beiträge zur Frage des Zwischenwirtes für Puccinia glumarum.Zeitschrift für Pflanzenkrankheiten (Pflanzenpathologie) und Pflanzenschutz, 1939, 49(10/11): 559–566 (in German)

[34] Mehmood S, Sajid M, Zhao J, Khan T, Zhan G, Huang L, Kang Z. Identification of berberis species collected from the himalayan region of Pakistan susceptible to Puccinia striiformis f. sp. tritici. Plant Disease, 2019, 103(3): 461–467

[35] Zhao J, Zhao S L, Peng Y L, Qin J F, Huang L L, Kang Z S. Investigation on geographic distribution and identification of six Berberis spp.serving as alternate host for Puccinia striiformis f. sp. tritici in Linzhi,Tibet. Acta Phytopathologica Sinica, 2016, 46(1): 103–111 (in Chinese)

[36] Zhao J, Zhao Y Y, Li Q, Huang L L, Kang Z S. Identification of Berberis germanensis as an alternate host of Puccinia striiformis f. sp. tritici under artificial conditions. Acta Phytopathologica Sinica, 2017, 47(2): 274–277 (in Chinese)

[37] Du Z M, Yao Q, Huang S J, Yan J H, Hou L, Guo Q Y, Zhao J, Kang Z S. Investigation and identification of barberry as alternate hosts for Puccinia striiformis f. sp. tritici in eastern Qinghai. Acta Phytopathologica Sinica, 2019, 49(3): 370–378 (in Chinese)

[38] Li S N, Chen W, Ma X Y, Tian X X, Liu Y, Huang L L, Kang Z S, Zhao J. Identification of eight Berberis species from the Yunnan-Guizhou plateau as aecial hosts for Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen. Journal of Integrative Agriculture, 2021, 20(6): 1563–1569

[39] Chen W, Zhang Z, Chen X, Meng Y, Huang L, Kang Z, Zhao J. Field production, germinability, and survival of Puccinia striiformis f. sp. tritici teliospores in China. Plant Disease, 2020: PDIS-09-20-2018-RE

[40] Wright R G, Lennard J H. Mitosis in Puccinia striiformis: 1. Light microscopy. Transactions of the British Mycological Society, 1978, 70(1): 91–98

[41] Wang M N, Chen X M. Barberry does not function as an alternate host for Puccinia striiformis f. sp. tritici in the U. S. Pacific Northwest due to teliospore degradation and barberry phenology. Plant Disease, 2015, 99(11): 1500–1506

[42] Wan A M, Wang M N, Chen X M. Variation in telial formation of Puccinia striiformis in the United States. American Journal of Plant Sciences, 2019, 10(05): 826–849

[43] Zadoks T C. Epidemiology of wheat rust in Europe. International Journal of Pest Management B, 1967, 13(1): 29–46

[44] Brown J K M, Hovmøller M S. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science, 2002, 297(5581): 537–541

[45] Sharp E L. Atmospheric ions and germination of uredospores of Puccinia striiformis. Science, 1967, 156(3780): 1359–1360

[46] Maddison A C, Manners J G. Sunlight and viability of cereal rust uredospores. Transactions of the British Mycological Society, 1972, 59(3): 429–443

[47] Xie S X, Wang K N, Chen Y L, Chen W Q. Preliminary study on the relationship between transport of wheat stripe rust and upper air current in China. Acta Phytopathologica Sinica, 1993, 23(3): 203–209 (in Chinese)

[48] Zeng S M, Luo Y. Long-distance spread and interregional epidemics of wheat stripe rust in China. Plant Disease, 2006, 90(8): 980–988

[49] Li Z Q, Liu H W. Preliminary study of development patterns of wheat stripe rust in Shaanxi, Gansu, and Qinghai. Journal of Northwest A&F University (Natural Science Edition), 1956, (4): 1–18 (in Chinese)

[50] Wang J Q, Lu J X, Liu S J, Dai S K, Liu S Z. Preliminary study on over-summering patterns of the wheat stripe rust pathogen in southern Gansu. Acta Phytopathologica Sinica, 1965, 8(1): 1–8 (in Chinese)

[51] Liu X K, Hong X W, Xie S X, Song W Z, Liu S X. A preliminary study on the over-summering of Puccinia striiformis in South Longnan. Acta Phytopathologica Sinica, 1984, 14(1): 9–16 (in Chinese)

[52] Yang X B, Zeng S M. Detecting patterns of wheat stripe rust pandemics in time and space. Phytopathology, 1992, 82(5): 571–576

[53] Zeng S M. On the mathematic analysis of the epiphytotics of wheat stripe rust. Acta Phytopathologica Sinica, 1962, 1(1): 35–48 (in Chinese)

[54] Chen W Q, Wu L R, Liu T G, Xu S C, Jin S L, Peng Y L, Wang B T. Race dynamics, diversity, and virulence evolution in Puccinia striiformis f. sp tritici, the causal agent of wheat stripe rust in China from 2003 to 2007. Plant Disease, 2009, 93(11): 1093–1101

[55] Han D J, Wang Q L, Chen X M, Zeng Q D, Wu J H, Xue W B, Zhan G M, Huang L L, Kang Z S. Emerging Yr26-virulent races of Puccinia striiformis f. sp. tritici are threatening wheat production in the Sichuan Basin, China. Plant Disease, 2015, 99(6): 754–760

[56] Liu H W, Meng X C. Analysis on breakdown of the resistance of wheat cultivar Bima 1. Shaanxi Journal of Agricultural Sciences, 1957, (06): 329–334 (in Chinese)

[57] Wan A, Zhao Z, Chen X, He Z, Jin S, Jia Q, Yao G, Yang J, Wang B, Li G, Bi Y, Yuan Z. Wheat stripe rust epidemic and virulence of Puccinia striiformis f. sp tritici in China in 2002. Plant Disease, 2004, 88(8): 896–904

[58] Zhang G S, Zhao Y Y, Kang Z S, Zhao J. First report of a Puccinia striiformis f. sp. tritici race virulent to wheat stripe rust resistance gene Yr5 in China. Plant Disease, 2020, 104(1): 284

[59] Han D J, Kang Z S. Current status and future strategy in breeding wheat for resistance to stripe rust in China. Plant Protection, 2018, 44(5): 1–12

[60] Wan A M, Chen X M, He Z H. Wheat stripe rust in China. Australian Journal of Agricultural Research, 2007, 58(6): 605–619

[61] Fan S Q, Xie X S, Li F, Yin Q Y, Zheng W Y. Forecast model for prevalent stripe rust in winter wheat in Shanxi Province. Chinese Journal of Eco-Agriculture, 2007, 15(4): 113–115 (in Chinese)

[62] Liu T G, Peng Y L, Chen W Q, Zhang Z Y. First detection of virulence in Puccinia striiformis f. sp. tritici in China to resistance genes Yr24 (=Yr26) present in wheat cultivar Chuanmai 42. Plant Disease, 2010, 94(9): 1163

[63] Salcedo A, Rutter W, Wang S, Akhunova A, Bolus S, Chao S, Anderson N, De Soto M F, Rouse M, Szabo L, Bowden R L, Dubcovsky J, Akhunov E. Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99. Science, 2017, 358(6370): 1604–1606

[64] Chen J, Upadhyaya N M, Ortiz D, Sperschneider J, Li F, Bouton C, Breen S, Dong C, Xu B, Zhang X, Mago R, Newell K, Xia X, Bernoux M, Taylor J M, Steffenson B, Jin Y, Zhang P, Kanyuka K, Figueroa M, Ellis J G, Park R F, Dodds P N. Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science, 2017, 358(6370): 1607–1610

[65] Jing J X, Shang H S, Li Z Q. The biological effects of ~⁽⁶⁰⁾Coγ-ray irradiation on stripe rust of wheat. Journal of Nuclear Agricultural Sciences, 1992, 6(2): 116–120 (in Chinese)

[66] Wang X L, Zhu F, Huang L L, Wei G R, Kang Z S. Effects of ultraviolet radiation on pathogenicity mutation of Puccinia striiformis f. sp. tritici. Journal of Nuclear Agricultural Sciences, 2009, 23(03): 375–379 (in Chinese)

[67] Shang H S, Jing J X, Li Z Q. Mutations induced ultraviolet radiation affecting virulence in Puccinia striiformis. Acta Phytopathologica Sinica, 1994, 24(04): 347–351 (in Chinese)

[68] Yao Q Y, Wang G F, Xu Z B, Wang M N, Wang Y, Jing J X. Virulent mutant in Puccinia striiformis induced by ethyl methyl sulfomar(EMS). Journal of Northwest A&F University (Natural Science Edition), 2006, 34(06): 120–123 (in Chinese)

[69] Kang Z S, Li Z Q, Shang H S. On the screening of new heterocaryons of wheat stripe rust and its nucleal dissociation. Acta Phytopathologica Sinica, 1994, 24(02): 101–105

[70] Little R, Manners J G. Somatic recombination in yellow rust of wheat (Puccinia striiformis). Transactions of the British Mycological Society, 1969, 53(2): 251–258

[71] Goddard M V. The production of a new race, 105 E 137 of Puccinia striiformis in glasshouse experiments. Transactions of the British Mycological Society, 1976, 67(3): 395–398

[72] Chen W Q, Xu S C, Wu L R. Epidemiology and sustainable management of wheat stripe rust caused by Puccinia striiformis West. in China: a historical retrospect and prospect. Scientia Agricultura Sinica, 2007, 40(Suppl): 3107–3113 (in Chinese)

[73] Tang C L, Xu Q, Zhao M X, Wang X J, Kang Z S. Understanding the lifestyles and pathogenicity mechanisms of obligate biotrophic fungi in wheat: the emerging genomics era. Crop Journal, 2018, 6(1): 60–67

[74] Bai B, Du J Y, Lu Q L, He C Y, Zhang L J, Zhou G, Xia X C, He Z H, Wang C S. Effective resistance to wheat stripe rust in a region with high disease pressure. Plant Disease, 2014, 98(7): 891–897

[75] Derevnina L, Michelmore R W. Wheat rusts never sleep but neither do sequencers: will pathogenomics transform the way plant diseases are managed? Genome Biology, 2015, 16(1): 44

[76] Hu X P, Yang Z W, Li Z Q, Deng Z Y, Ke C H. Studies on the prediction of wheat stripe rust epidemics in Hanzhong district of Shaanxi Province. Journal of Northeast Agricultural University, 2000, 28(2): 18–21 (Natural Science Edition)

[77] Xiao Z Q, Li Z M, Fan M, Zhang Y, Ma S J. Prediction model on stripe rust influence extent of winter wheat in Longnan mountain area. Chinese Journal of Agrometeorology, 2007, 28(3): 350–353

[78] Ngugi L C, Abelwahab M, Abo-Zahhad M. Recent advances in image processing techniques for automated leaf pest and disease recognition—a review. Information Processing in Agriculture, 2021, 8(1): 27–51

[79] Naik H S, Zhang J, Lofquist A, Assefa T, Sarkar S, Ackerman D, Singh A, Singh A K, Ganapathysubramanian B. A real-time phenotyping framework using machine learning for plant stress severity rating in soybean. Plant Methods, 2017, 13(1): 23

[80] Abd El-Ghany N M, Abd El-Aziz S E, Marei S S. A review: application of remote sensing as a promising strategy for insect pests and diseases management. Environmental Science and Pollution Research International, 2020, 27(27): 33503–33515

[81] Johannes A, Picon A, AlVarez-Gila A, Echazarra J, Rodriguez-Vaamonde S, Navajas A D, Ortiz-Barredo A. Automatic plant disease diagnosis using mobile capture devices, applied on a wheat use case. Computers and Electronics in Agriculture, 2017, 138: 200–209

[82] Bebronne R, Carlier A, Meurs R, Leemans V, Vermeulen P, Dumont B, Mercatoris B. In-field proximal sensing of septoria tritici blotch, stripe rust and brown rust in winter wheat by means of reflectance and textural features from multispectral imagery. Biosystems Engineering, 2020, 197: 257–269

[83] Lei Y, Han D J, Zeng Q D, He D J. Grading method of disease severity of wheat stripe rust based on hyperspectral imaging technology. Transactions of the Chinese Society for Agricultural Machinery, 2018, 49(5): 226–232 (in Chinese)

[84] National Bureau of Statistics (NBS). The usage of agricultural chemicals. Available at NBS website on November 2, 2020

[85] He X K. Rapid development of unmanned aerial vehicles (UAV) for plant protection and application technology in China. Outlooks on Pest Management, 2018, 29(4): 162–167

[86] Zhang J Q, Liu B, Chen W Q, Liu T G, Gao L. Temperature- sensitivity of population of Puccinia striiformis Westend. Acta Phytopathologica Sinica, 2013, 43(1): 89–90 (in Chinese)

[87] Line R F, Chen X M. Successes in breeding for and managing durable resistance to wheat rusts. Plant Disease, 1995, 79(12): 1254–1255

[88] Yu R, Jin Y G, Wu S S, Wu J H, Wang Q L, Zeng Q D, Liu S J, Xia Z H, Wang X J, Kang Z S, Han D J. Stripe rust resistance of candidate cultivars from south Yellow and Huai valley facultative wheat region in China. Journal of Triticeae Crops, 2020, 40(3): 278–284 (in Chinese)

[89] Zeng Q D, Han D J, Wang Q L, Yuan F P, Wu J H, Zhang L, Wang X J, Huang L L, Chen X M, Kang Z S. Stripe rust resistance and genes in Chinese wheat cultivars and breeding lines. Euphytica, 2014, 196(2): 271–284

[90] Qie Y, Liu Y, Wang M, Li X, See D R, An D, Chen X. Development, validation, and re-selection of wheat lines with pyramided genes Yr64 and Yr15 linked on the short arm of chromosome 1B for resistance to stripe rust. Plant Disease, 2019, 103(1): 51–58

[91] Bariana H S, Brown G N, Bansal U K, Miah H, Standen G E, Lu M. Breeding triple rust resistant wheat cultivars for Australia using conventional and marker-assisted selection technologies. Australian Journal of Agricultural Research, 2007, 58(6): 576–587

[92] Chen X. Review article: high-temperature adult-plant resistance, key for sustainable control of stripe rust. American Journal of Plant Sciences, 2013, 04(03): 608–627

[93] Risk J M, Selter L L, Chauhan H, Krattinger S G, Kumlehn J, Hensel G, Viccars L A, Richardson T M, Buesing G, Troller A, Lagudah E S, Keller B. The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotechnology Journal, 2013, 11(7): 847–854

[94] Krattinger S G, Sucher J, Selter L L, Chauhan H, Zhou B, Tang M, Upadhyaya N M, Mieulet D, Guiderdoni E, Weidenbach D, Schaffrath U, Lagudah E S, Keller B. The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnology Journal, 2016, 14(5): 1261–1268

[95] 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. Nature Genetics, 2015, 47(12): 1494–1498

[96] Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J L. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology, 2014, 32(9): 947–951

[97] Nekrasov V, Wang C, Win J, Lanz C, Weigel D, Kamoun S. Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Scientific Reports, 2017, 7(1): 482

[98] Zhang Y, Bai Y, Wu G, Zou S, Chen Y, Gao C, Tang D. Simultaneous modification of three homoeologs of TaEDR1 by genome editing enhances powdery mildew resistance in wheat. Plant Journal, 2017, 91(4): 714–724

[99] Zhu X, Qi T, Yang Q, He F, Tan C, Ma W, Voegele R T, Kang Z, Guo J. Host-induced gene silencing of the MAPKK gene PsFUZ7 confers stable resistance to wheat stripe rust. Plant Physiology, 2017, 175(4): 1853–1863

[100] Zhu H, Li C, Gao C. Applications of CRISPR-Cas in agriculture and plant biotechnology. Nature Reviews. Molecular Cell Biology, 2020, 21(11): 661–677

Acknowledgements

The authors acknowledge support from the National Natural Science Foundation of China (31620103913), the “111 Project” from the Ministry of Education of China (BP0719026), and the Natural Science Basic Research Plan in Shaanxi Province of China (2019JCW-18). The authors are grateful to Professor R. A. McIntosh, Plant Breeding Institute, University of Sydney, Australia, for critical review of this manuscript.

Compliance with ethics guidelines

Qingdong Zeng, Jie Zhao, Jianhui Wu, Gangming Zhan, Dejun Han, and Zhensheng Kang declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2021. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)