The TaFIM1 gene mediates wheat resistance against Puccinia striiformis f. sp. tritici and responds to abiotic stress

doi:10.1016/S2095-3119(20)63276-2

摘要/Abstract

摘要：

丝束蛋白（fimbrin）是肌动蛋白细胞骨架的调节因子，参与并控制多种组织和细胞的生理生化和发育过程。然而，fimbrin在对病原菌防御中，特别是在小麦抗条锈病中的作用研究匮乏，其机制尚待阐明。本研究以小麦品种水源11（Suwon 11）与条锈菌（Puccinia striiformis f. sp. tritici，Pst）生理小种CYR23组成非亲和互作，与生理小种CYR31组成成亲和互作，利用实时荧光定量 PCR 技术（qRT-PCR）对TaFIM1基因参与小麦抗条锈病的功能进行初步分析；对在非生物胁迫和施用外源激素处理TaFIM1基因的表达特征进行分析；通过病毒诱导的基因沉默（BSMV-VIGS）技术，验证TaFIM1在小麦抗条锈病中的功能。获得以下研究结果：TaFIM1在非亲和互作中的表达量显著上调，且在48 h表达量达到峰值，是对照0 h的6.0倍；在亲和互作中，TaFIM1的表达量无明显变化。TaFIM1能够响应不同非生物胁迫，在高温（Hot）、低温（Cool）、盐（NaCl）和干旱（PEG6000）胁迫下诱导TaFIM1基因表达量上调。BSMV-VIGS试验结果显示，借助大麦条纹花叶病毒对TaFIM1基因进行诱导沉默。对沉默成功的小麦植株分别接种条锈菌CYR23和CYR31。在非亲和互作中，沉默植株的抗病性降低，叶片上出现少量的夏孢子堆；在亲和互作中，与对照相比，叶片上的夏孢子堆数量增加，沉默植株的感病性增强。组织学观察发现，在48 h和120 h，TaFIM1沉默植株叶片中菌丝分支数和菌丝长度高于对照，在120 h基因沉默植株叶片中菌落面积显著高于对照组，表明TaFIM1沉默后小麦植株与对照相比感病性增强，进一步说明TaFIM1参与植物的抗病性。因此，TaFIM1与植物抗病性相关，在小麦抵抗条锈病的侵染过程中响应正调控作用。本研究为理解fimbrin在小麦中的作用提供了新的见解。

Abstract:

Fimbrin, a regulator of actin cytoskeletal dynamics that participates in numerous physiological and biochemical processes, controls multiple developmental processes in a variety of tissues and cell types. However, the role of fimbrin in pathogen defense of wheat and the mechanisms have not been well studied. Here, we investigated that the expression of TaFIM1 gene of wheat was significantly induced in response to avirulent race of Puccinia striiformis f. sp. tritici (Pst) and silencing of TaFIM1 by virus-induced gene silencing method. The results show that silencing of TaFIM1 resulted in a reduction of resistance against the stripe rust indicated by both phenotypes and a histological examination of Pst growth. Additionally, the expression level of TaFIM1 gene was up-regulated under abiotic stresses. These findings suggest that TaFIM1 functions as a positive regulator of pathogen resistance of wheat plants and response to abiotic stress. Our work may show new light on understanding the roles of fimbrin in wheat.

Key words: wheat , Puccinia striiformis f. sp. tritici , fimbrin , disease resistance , abiotic stress

. [J]. Journal of Integrative Agriculture, 2021, 20(7): 1849-1857.

SHI Bei-bei, WANG Juan, GAO Hai-feng, ZHANG Xiao-juan, WANG Yang, MA Qing. The TaFIM1 gene mediates wheat resistance against Puccinia striiformis f. sp. tritici and responds to abiotic stress[J]. Journal of Integrative Agriculture, 2021, 20(7): 1849-1857.

参考文献

Adams A E M, Botstein D, Drubin D G. 1991. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature, 354, 404–408.
Adams A E M, Shen W Y, Lin C S, Leavitt J, Matsudaira P. 1995. Isoformspecific complementation of the yeast sac6 null mutation by human fimbrin. Molecular and Cellular Biology, 15, 69–75.
Alazem M, Lin N S. 2015. Roles of plant hormones in the regulation of host-virus interactions. Molecular Plant Pathology, 16, 529–540.
Beddow J M, Pardey P G, Chai Y, Hurley T M, Kriticos D J, Braun H J, Park R F, Cuddy W S, Yonow T. 2015. Research investment implications of shifts in the global geography of wheat stripe rust. Nature Plants, 1, 1–32.
Chen P D, Qi L L, Zhou B, Zhang S Z, Liu D J. 1995. Development and molecular cytogenetic analysis of wheat-Haynaldia villosa 6VS/6AL translocation lines specifying resistance to powdery mildew. Theoretical and Applied Genetics, 91, 1125–1128.
Cruz-Ortega R. 1997. cDNA clones encoding 1,3-beta-glucanase and a fimbrin-like cytoskeletal protein are induced by AI toxicity in wheat roots. Plant Physiology, 114, 1453–1460.
Dangl J L, Horvath D M, Staskawicz B J. 2013. Pivoting the plant immune system from dissection to deployment. Science, 341, 746–751.
Day B, Henty J L, Porter K J, Staiger C J. 2011. The pathogen-actin connection: A platform for defense signaling in plants. Annual Review of Phytopathology, 49, 483–506.
Dodds P N, Rathjen J P. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics, 11, 539–548.
Dong Z, Hegarty J M, Zhang J, Zhang W, Dubcovsky J. 2017. Validation and characterization of a QTL for adult plant resistance to stripe rust on wheat chromosome arm 6BS (Yr78). Theoretical and Applied Genetics, 130, 2127–2137.
Fujiwara I, Takahashi S, Tadakuma H, Funatsu T, Ishiwata S I. 2002. Microscopic analysis of polymerization dynamics with individual actin filaments. Nature Cell Biology, 4, 666–673.
Galá J E, Collmer A. 1999. Type III secretion machines: Bacterial devices for protein delivery into host cells. Science, 284, 1322–1328.
Gessese M, Bariana H, Wong D, Hayden M, Bansal U. 2019. Molecular mapping of stripe rust resistance gene Yr81 in a common wheat landrace Aus27430. Plant Disease, 103, 1166–1171.
Hein I, Barciszewska-Pacak M, Hrubikova K, Williamson S, Dinesen M, Soenderby I E, Sundar S, Jarmolowski A, Shirasu K, Lacomme C. 2005. Virus-induced gene silencing-based functional characterization of genes associated with powdery mildew resistance in barley. Plant Physiology, 138, 2155–2164.
Henty-Ridilla J L, Shimono M, Li J, Chang J H, Day B, Staiger C J. 2013. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathogens, 9, 32–45.
Huang G T, Ma S L, Bai L P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z F. 2012. Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 39, 969–987.
Jones J D G, Dangl J L. 2006. The plant immune system. Nature, 444, 323–329.
Kang Z S, Li Z Q. 1984. Discovery of a normal T. type new pathogenic strain to Lovrin 10. Journal of Northwest Sci-tech University of Agriculture and Forestry (Natural Science Edition, 4, 18–28. (in Chiense)
Klein M G, Shi W, Ramagopal U, Tseng Y, Wirtz D, Kovar D R, Staiger C J, Almo S C. 2004. Structure of the actin crosslinking core of fimbrin. Structure, 12, 999–1013.
Kovar D R, Gibbon B C, Staiger M C J. 2001. Fluorescently-labeled fimbrin decorates a dynamic actin filament network in live plant cells. Planta, 213, 390–395.
Lazniewska J, Macioszek V K, Kononowicz A K. 2012. Plant-fungus interface: The role of surface structures in plant resistance and susceptibility to pathogenic fungi. Physiological & Molecular Plant Pathology, 78, 24–30.
Li J, Henty-Ridilla J L, Staiger B H, Day B, Staiger C J. 2015. Capping protein integrates multiple MAMP signaling pathways to modulate actin dynamics during plant innate immunity. Nature Communications, 6, 7206–7215.
Liu B. 2011. The Plant Cytoskeleton. Springer, New York.
Macho A P, Zipfel C. 2015. Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Current Opinion in Microbiology, 23, 14–22.
Marais F, Marais A, McCallum B, Pretorius Z. 2009. Transfer of leaf rust and stripe rust resistance genes Lr62 and Yr42 from Aegilops neglecta Req. ex Bertol. to common wheat. Crop Science, 49, 871–879.
Marais G F, McCallum B, Marais A S. 2006. Leaf rust and stripe rust resistance genes derived from Aegilops sharonensis. Euphytica, 149, 373–380.
Marais G F, Pretorius Z A, Marais A S, Wellings C R. 2003. Transfer of rust resistance genes from Triticum species to common wheat. South African Journal of Plant and Soil, 20, 193–198.
Minsavage G V, Dahlbeck D, Whalen M C, Kearney B, Bonas U, Staskawicz B J. 1990. Gene-for-gene relationships specifying disease resistance in Xanthomonas campestris pv vesicatoria-pepper interactions. Molecular Plant Microbe Interactions, 3, 41–48.
Miyakawa T, Shinomiya H, Yumoto F. 2012. Different Ca2+-sensitivities between the EF-hands of T- and L-plastins. Biochemical & Biophysical Research Communications, 429, 137–141.
Niirnberger T, Nennstiel D, Jabs T, Sacks W R, Hahlbrock K, Scheel D. 1994. Highaffinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell, 78, 60–72.
Ouellet F, Carpentier E, Cope M J T, Monroy A F, Sarhan F. 2001. Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiology, 125, 360–368.
Petty I T, French R, Jones R W, Jackson A O. 1990. Identification of barley stripe mosaic virus genes involved in viral RNA replication and systemic movement. The EMBO Journal, 9, 3453–3457.
Qi T, Wang J, Sun Q X, Day B, Guo J, Ma Q. 2017. TaARPC3, contributes to wheat resistance against the stripe rust fungus. Frontiers in Plant Science, 8, 1–13.
Shinomiya H. 2012. Plastin family of actin-bundling proteins: its functions in leukocytes, neurons, intestines, and cancer. International Journal of Cell Biology, 2012, 213–235.
Singh R P, Singh P K, Rutkoski J, Hodson D P, He X, JøRgenssen L N, Hovmøller M S, Espino J H. 2016. Disease impact on wheat yield potential and prospects of genetic control. Annual Review of Phytopathology, 54, 615–635.
Su H, Zhu J S, Cai C, Pei W K, Wang J J, Dong H J, Ren H Y. 2012. Fimbrin1 is involved in lily pollen tube growth by stabilizing the actin fringe. The Plant Cell, 24, 4539–4554.
Sugiyama Y, Nagashima Y, Wakazaki M, Sato M, Toyooka K, Fukuda H, Oda Y. 2019. A Rho-actin signaling pathway shapes cell wall boundaries in Arabidopsis xylem vessels. Nature Communications, 10, 468–480.
Sun G Z, Feng C J, Guo J, Zhang A C, Xu Y L, Wang Y, Day B, Ma Q. 2019. The tomato Arp2/3 complex is required for resistance to the powdery mildew fungus Oidium neolycopersici. Plant, Cell & Environment, 10, 135–149.
Sun H, Qiao Z, Chua K P, Tursic A, Liu X, Gao Y G. 2018. Profilin negatively regulates formin-mediated actin assembly to modulate PAMP-triggered plant immunity. Current Biology, 26, 177–195.
Uauy C, Brevis J C, Chen X, Khan I, Jackson L, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J. 2005. High-temperature adult-plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theoretical and Applied Genetics, 112, 97–105.
Vidali L, Mckenna S T, Hepler P K. 2001. Actin polymerization is essential for pollen tube growth. Molecular Biology of the Cell, 12, 2534–2545.
Wang J, Wang Y, Liu X J, Xu Y L, Ma Q. 2016. Microtubule polymerization functions in hypersensitive response and accumulation of H2O2 in wheat induced by the stripe rust. Biomed Research International, 3, 1–7.
Wang W, Wen Y, Berkey R, Xiao S. 2009. Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. The Plant Cell, 21, 2898–2913.
Wang X, Tang C, Zhang H, Xu J R, Liu B, Lv J, Han D, Huang L, Kang Z S. 2011. TaDAD2, a negative regulator of programmed cell death, is important for the interaction between wheat and the stripe rust fungus. Molecular Plant Microbe Interactions, 24, 79–90.
Wang X, Wang X, Feng H, Tang C, Bai P, Wei G, Huang L L, Kang Z S. 2012. TaMCA4, a novel wheat metacaspase gene functions in programmed cell death induced by the fungal pathogen Puccinia striiformis f. sp. tritici. Molecular Plant Microbe Interactions, 25, 755–764.
Wellings C R. 2011. Global status of stripe rust: A review of historical and current threats. Euphytica, 179, 129–141.
Yiping Q I, Tsuda K, Glazebrook J, Katagiri F. 2011. Physical association of pattern-triggered immunity (PTI) and effector-triggered immunity (ETI) immune receptors in Arabidopsis. Molecular Plant Pathology, 12, 702–708.
Zhang B, Hua Y, Wang J, Huo Y, Shimono M, Day B, Ma Q. 2017. TaADF4, an actin-depolymerizing factor from wheat, is required for resistance to the stripe rust pathogen Puccinia striiformis f. sp. tritici. Plant Journal, 89, 121–130.
Zhang M, Zhang R, Qu X, Huang S. 2016. Arabidopsis FIM5 decorates apical actin filaments and regulates their organization in the pollen tube. Journal of Experimental Botany, 67, 3407–3417.
Zheng Z, Gao T, Zhang Y, Hou Y, And J W, Zhou M. 2014. FgFim, a key protein regulating resistance to the fungicide js399-19, asexual and sexual development, stress responses and virulence in Fusarium graminearum. Molecular Plant Pathology, 15, 488–499.