Welcome to Acta Agronomica Sinica，

Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (1): 19-29.doi: 10.3724/SP.J.1006.2021.01050

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Overexpression of TaJRL53 enhances the Fusarium head blight resistance in wheat

CHEN Tong-Rui(), LUO Yan-Jun, ZHAO Pan-Ting, JIA Hai-Yan*(), MA Zheng-Qiang   

  1. College of Agriculture, Nanjing Agricultural University / State Key Laboratory for Crop Genetics and Germplasm Enhancement / Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing 210095, Jiangsu, China
  • Received:2020-06-17 Accepted:2020-09-13 Online:2021-01-12 Published:2020-09-30
  • Contact: JIA Hai-Yan E-mail:2017101089@njau.edu.cn;hyjia@njau.edu.cn
  • Supported by:
    National Key Research and Development Program of China(2016YFD0101004)

RichHTML376

34

PDF

1018

Abstract:

Jacalin-related lectins (JRLs) are a group of plant lectins with jacalin protein domain, which play important roles during plant response to biotic and abiotic stress. According their carbohydrate binding specificities, the JRLs were described as two types: galactose-binding acalins (gJRLs) and mannose-binding jacalins (mJRLs). Previous studies have shown that TaJRL53 encodes a protein with Jacalin and Dirigent domains and can be up-regulated by Fusarium graminearum infection. Wheat FHB induced by this pathogen is a disastrous disease, which not only reduces the grain yield, but also contains deoxynivalenol and other toxins, which seriously affect the health of human and livestock. To dissect the gene’s function in FHB resistance, we silenced and overexpressed the TaJRL53 in wheat respectively. As a result, attenuating TaJRL53 increased susceptibility to Fusarium graminearum. And susceptible wheat transformed with TaJRL53 over-expression showed higher Fusarium head blight resistance, the number of diseased spikelets (NDS) and length of diseased spike rachis (LDR) of transgenics wheat with TaJRL53 overexpression were significantly reduced than those of wild type. After Fusarium graminearum infection, the expression of ROS synthesis pathway, JA synthesis and signaling pathways marker genes, and disease related genes in TaJRL53 over-expression transgenic plants were higher than those in non-transgenic control. These results suggest that TaJRL53 enhanced the FHB resistance in wheat through regulating ROS synthesis pathway and JA signal transduction pathways. This study enhanced the understanding of wheat JRLs family genes’ function and laid a foundation for the mechanism dissection of TaJRL53 resistant to FHB in wheat.

Key words: wheat, Jacalin-related lectins, FHB resistance, ROS, JA pathway

Fig. 1

Scheme of the TaJRL53 overexpression vector"

Fig. 2

Tissue-specific expression of TaJRL53 A: seedling stage; B: flowering stage. Bar=50 μm."

Fig. 3

Expression of TaJRL53-GFP fusion protein in onion epidermal cells"

Fig. 4

The FHB resistance of spikes after TaJRL53 silenced A: Expression level of TaJRL53 in spike after inoculation with virus; B: Number of disease spikelet; C: Length of diseased rachides; D: Disease symptoms of spikes; The numbers in brackets show the number of samples. * and *** represent significant difference at level P < 0.05 and P < 0.001 (Student’s t-test)."

Fig. 5

PCR test and expression level of TaJRL53 in T0 transgenic plants with TaJRL53 overexpression M: marker; 1-6: transgenic plants from Bobwhite; 7: transgenic plant from PH691. PH: PH691; Bob: Bobwhite; H: H2O; P: positive control."

Fig. 6

FHB resistance of TaJRL53 overexpression transgenic plants A: inoculated leaf; B: lesion area; C: inoculated spike; D: number of diseases spikelets; E: length of diseased rachide. 1-5: transgenic plants from Bobwhite; 6: transgenic plant from Ph691. The numbers in brackets of B, D, and E show the number of samples. *, **, and ***: significant difference at P < 0.05, P < 0.01, and P < 0.001 (Student’s t-test)."

Fig. 7

Expression of marker genes in resistance signaling pathways A-C: marker genes in JA singnal pathway; D, H, I: pathogenesis-related genes; E, F: ROS biosynthesis-related genes; G: ROS transport-related genes; J-L: SA singnal pathway-related genes; M, N: SA biosynthesis-related genes; O: lignin biosynthesis genes; Bob: Bobwhite; 1-4: transgenic plants from Bobwhite; * and **: significant difference at P < 0.05 and P < 0.01 (Student’s t-test)."

[1] Chisholm S T, Coaker G, Day B, Staskawicz B J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 2006,124:803-814.
doi: 10.1016/j.cell.2006.02.008 pmid: 16497589
[2] Jones J D, Dangl J L. The plant immune system. Nature, 2006,444:323-329.
pmid: 17108957
[3] 李圣军. 世界小麦产量格局及演变分析. 粮食问题研究, 2017, (6):9-15.
Li S J. Analysis of world wheat production, marketing pattern and evolution. Grain Issues Res, 2017, (6):9-15 (in Chinese).
[4] Gilbert J, Tekauz A. Review: recent developments in research on fusarium head blight of wheat in Canada. Can J Plant Pathol, 2000,22:1-8.
doi: 10.1080/07060660009501155
[5] Goswami R S, Kistler H C. Heading for disaster: Fusarium graminearum on cereal crops. Mol Plant Pathol, 2010,5:515-525.
pmid: 20565626
[6] Song M, Xu W Q, Xiang Y, Jia H Y, Zhang L X, Ma Z Q. Association of jacalin-related lectins with wheat responses to stresses revealed by transcriptional profiling. Plant Mol Biol, 2014,84:95-110.
doi: 10.1007/s11103-013-0121-5
[7] Jiang S Y, Ma Z, Ramachandran S. Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol, 2010,10:79.
doi: 10.1186/1471-2148-10-79 pmid: 20236552
[8] Van Damme E J M, Lannoo N, Peumans W J. Plant lectins. Adv Bot Res, 2008,48:107-209.
[9] 徐文琦. 小麦JRL凝集素基因的表达及TaJRL2.1的功能分析. 南京农业大学博士学位论文, 江苏南京, 2014.
Xu W Q. Expression and Function Analysis of TaJRL2.1 in Wheat. PhD Dissertation of Nanjing Agricultural University, Nanjing, Jiangsu, China, 2014 (in Chinese with English abstract).
[10] Azarkan M, Feller G, Vandenameele J, Herman R, El Mahyaoui R, auvage E, Vanden Broeck A, Matagne A, Charlier P, Kerff F. Biochemical and structural characterization of a mannose binding jacalin-related lectin with two-sugar binding sites from pineapple (Ananas comosus) stem. Sci Rep, 2018,8:11508.
pmid: 30065388
[11] Raval S, Gowda S B, Singh D D, Chandra N R. A database analysis of jacalin-like lectins: sequence-structure-function relationships. Glycobiology, 2004,14:1247-1263.
doi: 10.1093/glycob/cwh140 pmid: 15329359
[12] Ma Q H. Monocot chimeric jacalins: a novel sub family of plant lectins. Crit Rev Biotechnol, 2014,34:300-306.
doi: 10.3109/07388551.2013.793650 pmid: 23886351
[13] Esch L, Schaffrath U. An update on jacalin-like lectins and their role in pant defense. Int J Mol Sci, 2017,18:1592-1602.
doi: 10.3390/ijms18071592
[14] Ye X Y, Ng T B, Tsang P W, Wang J. Isolation of a homodimeric lectin with antifungal and antiviral activities from red kidney bean (Phaseolus vulgaris) seeds. J Protein Chem, 2001,20:367-375.
doi: 10.1023/a:1012276619686 pmid: 11732688
[15] Desclos-Theveniau M, Arnaud D, Huang T Y, Lin G J, Chen W Y, Lin Y C, Zimmerli L. The Arabidopsis lectin receptor kinase LecRK-V.5 represses stomatal immunity induced by Pseudomonas syringae pv. tomato DC3000. PLoS Pathog, 2012,8:e1002513.
doi: 10.1371/journal.ppat.1002513 pmid: 22346749
[16] Singh P, Kuo Y C, Mishra S, Tsai C H, Chen C C, Chen C W, Desclos-Theveniau M, Chu P W, Schulze B, Chinchilla D, Boller T, Zimmerli L. The lectin receptor Kinase-VI.2 is required for priming and positively regulates Arabidopsis pattern-triggered immunity. Plant Cell, 2012,24:1256-1270.
doi: 10.1105/tpc.112.095778
[17] Yamaji Y, Maejima K, Komatsu K, Shiraishi T, Okano Y, Himeno M, Sugawara K, Neriya Y, Minato N, Miura C, Hashimoto M, Namba S. Lectin-mediated resistance impairs plant virus infection at the cellular level. Plant Cell, 2012,24:778-793.
pmid: 22307853
[18] Sugawara K, Shiraishi T, Yoshida T, Fujita N, Netsu O, Yamaji Y, Namba S. A replicase of Potato Virus X acts as the resistance-breaking determinant for JAX1-mediated resistance. Mol Plant Microbe, 2013,26:1106-1129.
doi: 10.1094/MPMI-04-13-0094-R
[19] Hwang I S, Hwang B K. The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Plant Physiol, 2011,155:447-463.
pmid: 21205632
[20] Miya A, Albert P, Shinya T, Desak Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA, 2007,104:19613-19618.
[21] Wan J, Zhang X C, Neece D, Ramonell K M, Clough S, Kim S Y, Stacey M G, Stacey G. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell, 2008,20:471-481.
[22] Chisholm S T, Mahajan S K, Whitham S A, Yamamoto M L, Carrington J C. Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc Natl Acad Sci USA, 2001,97:489-494.
pmid: 10618445
[23] Chisholm S T, Parra M A, Anderberg R J, Carrington J C. Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol, 2001,127:1667-1675.
pmid: 11743111
[24] Cosson P, Sofer L, Schurdi-Levraud V, Revers F. A member of a new plant gene family encoding a Meprin and TRAF homology (MATH) domain-containing protein is involved in restriction of long distance movement of plant viruses. Plant Signal Behave, 2010,5:1321-1323.
[25] Nagano A J, Fukao Y, Fujiwara M, Nishimura M, Hara- Nishimura I. Antagonistic jacalin-related lectins regulate the size of ER body-type β-glucosidase complexes in Arabidopsis thaliana. Plant Cell Physiol, 2008,49:969-980.
pmid: 18467340
[26] Weidenbach D, Esch L, Möller C, Hensel G, Kumlehn J, Höfle C, Hückelhoven R, Schaffrath U. Polarized defense against fungal pathogens is mediated by the jacalin-related lectin domain of modular Poaceae-specific proteins. Mol Plant, 2016,9:514-527.
doi: 10.1016/j.molp.2015.12.009 pmid: 26708413
[27] Han Y, Song L, Peng C L, Liu X, Liu L H, Zhang Y H, Wang W Z, Zhou J, Wang S H, Ebbole D, Wang Z H, Lu G D. A Magnaporthe chitinase interacts with a rice jacalin-related lectin to promote host colonization. Plant Physiol, 2019,179:1416-1430.
doi: 10.1104/pp.18.01594 pmid: 30696749
[28] Xiang Y, Song M, Wei Z Y, Tong J H, Zhang L X, Xiao L T, Ma Z Q, Wang Y. A jacalin-related lectin-like gene in wheat is a component of the plant defence system. J Exp Bot, 2011,62:5471-5483.
doi: 10.1093/jxb/err226 pmid: 21862481
[29] Goriach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel K H, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J. Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell, 1996,8:629-643.
doi: 10.1105/tpc.8.4.629 pmid: 8624439
[30] Subramanyam S, Smith D F, Clemens J C, Webb M A, Sardesai N, Williams C E. Functional characterization of HFR1, a high-mannose N-glycan-specific wheat lectin induced by Hessian fly larvae. Plant Physiol, 2008,147:1412-1426.
doi: 10.1104/pp.108.116145 pmid: 18467454
[31] Ma Q H, Tian B, Li Y L. Overexpression of a wheat jasmonate-regulated lectin increases pathogen resistance. Biochimie, 2010,92:187-193.
doi: 10.1016/j.biochi.2009.11.008 pmid: 19958808
[32] Krattinger S G, Keller B. Molecular genetics and evolution of disease resistance in cereals. New Phytol, 2016,212:320-332.
pmid: 27427289
[33] Han Y J, Zhong Z H, Song L L, Olsson Stefan, Wang Z H, Lu G D. Evolutionary analysis of plant jacalin-related lectins (JRLs) family and expression of rice JRLs in response to Magnaporthe oryzae. J Integr Agric, 2018,17:60345-60347.
[34] 宋敏. 小麦JRL和DIR基因家族的鉴定和分析. 南京农业大学博士学位论文, 江苏南京, 2013.
Song M. Identification and Analysis of JRL and DIR Gene Family. PhD Dissertation of Nanjing Agricultural University, Jiangsu, Nanjing, China, 2013.
[35] Livak K J, Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) Method. Methods, 2001,25:402-408.
pmid: 11846609
[36] Ding L N, Xu H B, Yi H Y, Yang L M, Kong Z X, Zhang L X, Xue S L, Jia H Y, Ma Z Q. Resistance to hemi-biotrophic F. graminearum infection is associated with coordinated and ordered expression of diverse defense signaling pathways. PLoS One, 2011,6:e19008.
pmid: 21533105
[37] Vasil I K, Vasil V. Transformation of wheat via particle bombardment. Meth Mol Biol, 2006,318:273-283.
[38] Ma Z Q, Sorrells M E. Genetic analysis of fertility restoration in wheat using restriction fragment length polymorphisms. Crop Sci, 1995,3:1137-1143.
[39] Li G Q, Zhou J Y, Jia H Y, Gao Z X, Fan M, Luo Y J, Zhao P T, Xue S L, Li N, Yuan Y, Ma S W, Kong Z X, Jia L, An X, Jiang G, Liu W X, Cao W J, Zhang R R, Fan J C, Xu X W, Liu Y F, Kong Q Q, Zheng S H, Wang Y, Qin B, Cao S Y, Ding Y X, Shi J X, Yan H S, Wang X, Ran C F, Ma Z Q. Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight. Nat Genet, 2019,51:1106-1112.
doi: 10.1038/s41588-019-0426-7 pmid: 31182810
[40] Abebe T, Skadsen R W, Kaeppler H F. A proximal upstream sequence controls tissue-specific expression of Lem2, a salicylate-inducible barley lectin-like gene. Planta, 2005,21:170-183.
[41] Jia F, Rock C D. Jacalin lectin At5g28520 is regulated by ABA and miR846. Plant Signal Behav, 2013,8:e24563.
doi: 10.4161/psb.24563 pmid: 23603955
[42] Xing L J, Li J, Xu Y Y, Xu Z H, Chong K. Phosphorylation modification of wheat lectin VER2 is associated with vernalization-induced O-GlcNAc signaling and intracellular modlity. PLoS One, 2009,4:e4854.
doi: 10.1371/journal.pone.0004854 pmid: 19287503
[43] He X, Li L, Xu H, Xi J, Cao X, Xu H, Rong S, Dong Y, Wang C, Chen R, Xu J, Gao X, Xu Z. A rice jacalin-related mannose- binding lectin gene, OsJRL, enhances Escherichia coli viability under high salinity stress and improves salinity tolerance of rice. Plant Biol (Stuttg), 2017,19:257-267.
pmid: 27718311
[44] Zhang H L, Deng C, Yao J, Zhang Y L, Zhang Y N, Deng S R, Zhao N, Sa G, Zhou X Y, Lu C F, Lin S Z, Zhao R, Chen S L. Populus euphratica JRL mediates ABA response, ionic and ROS homeostasis in Arabidopsis under salt stress. Int J Mol Sci, 2019,20:815.
doi: 10.3390/ijms20040815
[45] Weidenbach D, Esch L, Möller C, Hensel G, Kumlehn J, Höfle C, Hückelhoven R, Schaffrath U. Polarized defense against fungal pathogens is mediated by the jacalin-related lectin domain of modular Poaceae-specific proteins. Mol Plant, 2016,9:514-527.
doi: 10.1016/j.molp.2015.12.009 pmid: 26708413
[46] Beckers G J M, Spoel S H. Fine-tuning plant defense signaling: salicylate versus jasmonate. Plant Biol, 2006,8:1-10.
doi: 10.1055/s-2005-872705 pmid: 16435264
[47] Glazebrook J, Chen W, Estes B, Chang H S, Nawrath C, Metraux J P, Zhu T, Katagiri F. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J, 2003, 34:217-228.
doi: 10.1046/j.1365-313x.2003.01717.x pmid: 12694596
[48] Khaledi N, Taheri P, Falahati-Rastegar M. Reactive oxygen species and antioxidant system responses in wheat cultivars during interaction with Fusarium species. Australas Plant Pathol, 2016,45:653-670.
doi: 10.1007/s13313-016-0455-y
[1] HU Wen-Jing, LI Dong-Sheng, YI Xin, ZHANG Chun-Mei, ZHANG Yong. Molecular mapping and validation of quantitative trait loci for spike-related traits and plant height in wheat [J]. Acta Agronomica Sinica, 2022, 48(6): 1346-1356.
[2] GUO Xing-Yu, LIU Peng-Zhao, WANG Rui, WANG Xiao-Li, LI Jun. Response of winter wheat yield, nitrogen use efficiency and soil nitrogen balance to rainfall types and nitrogen application rate in dryland [J]. Acta Agronomica Sinica, 2022, 48(5): 1262-1272.
[3] PENG Xi-Hong, CHEN Ping, DU Qing, YANG Xue-Li, REN Jun-Bo, ZHENG Ben-Chuan, LUO Kai, XIE Chen, LEI Lu, YONG Tai-Wen, YANG Wen-Yu. Effects of reduced nitrogen application on soil aeration and root nodule growth of relay strip intercropping soybean [J]. Acta Agronomica Sinica, 2022, 48(5): 1199-1209.
[4] LEI Xin-Hui, WAN Chen-Xi, TAO Jin-Cai, LENG Jia-Jun, WU Yi-Xin, WANG Jia-Le, WANG Peng-Ke, YANG Qing-Hua, FENG Bai-Li, GAO Jin-Feng. Effects of soaking seeds with MT and EBR on germination and seedling growth in buckwheat under salt stress [J]. Acta Agronomica Sinica, 2022, 48(5): 1210-1221.
[5] FU Mei-Yu, XIONG Hong-Chun, ZHOU Chun-Yun, GUO Hui-Jun, XIE Yong-Dun, ZHAO Lin-Shu, GU Jia-Yu, ZHAO Shi-Rong, DING Yu-Ping, XU Yan-Hao, LIU Lu-Xiang. Genetic analysis of wheat dwarf mutant je0098 and molecular mapping of dwarfing gene [J]. Acta Agronomica Sinica, 2022, 48(3): 580-589.
[6] FENG Jian-Chao, XU Bei-Ming, JIANG Xue-Li, HU Hai-Zhou, MA Ying, WANG Chen-Yang, WANG Yong-Hua, MA Dong-Yun. Distribution of phenolic compounds and antioxidant activities in layered grinding wheat flour and the regulation effect of nitrogen fertilizer application [J]. Acta Agronomica Sinica, 2022, 48(3): 704-715.
[7] LIU Yun-Jing, ZHENG Fei-Na, ZHANG Xiu, CHU Jin-Peng, YU Hai-Tao, DAI Xing-Long, HE Ming-Rong. Effects of wide range sowing on grain yield, quality, and nitrogen use of strong gluten wheat [J]. Acta Agronomica Sinica, 2022, 48(3): 716-725.
[8] ZHENG Xiang-Hua, YE Jun-Hua, CHENG Chao-Ping, WEI Xing-Hua, YE Xin-Fu, YANG Yao-Long. Xian-geng identification by SNP markers in Oryza sativa L. [J]. Acta Agronomica Sinica, 2022, 48(2): 342-352.
[9] YAN Yan, ZHANG Yu-Shi, LIU Chu-Rong, REN Dan-Yang, LIU Hong-Run, LIU Xue-Qing, ZHANG Ming-Cai, LI Zhao-Hu. Variety matching and resource use efficiency of the winter wheat-summer maize “double late” cropping system [J]. Acta Agronomica Sinica, 2022, 48(2): 423-436.
[10] WANG Yang-Yang, HE Li, REN De-Chao, DUAN Jian-Zhao, HU Xin, LIU Wan-Dai, GU Tian-Cai, WANG Yong-Hua, FENG Wei. Evaluations of winter wheat late frost damage under different water based on principal component-cluster analysis [J]. Acta Agronomica Sinica, 2022, 48(2): 448-462.
[11] XIE Cheng-Hui, MA Hai-Zhao, XU Hong-Wei, XU Xi-Yang, RUAN Guo-Bing, GUO Zheng-Yan, NING Yong-Pei, FENG Yong-Zhong, YANG Gai-He, REN Guang-Xin. Effects of nitrogen rate on growth, grain yield, and nitrogen utilization of multiple cropping proso millet after spring-wheat in Irrigation Area of Ningxia [J]. Acta Agronomica Sinica, 2022, 48(2): 463-477.
[12] CHEN Xin-Yi, SONG Yu-Hang, ZHANG Meng-Han, LI Xiao-Yan, LI Hua, WANG Yue-Xia, QI Xue-Li. Effects of water deficit on physiology and biochemistry of seedlings of different wheat varieties and the alleviation effect of exogenous application of 5-aminolevulinic acid [J]. Acta Agronomica Sinica, 2022, 48(2): 478-487.
[13] XU Long-Long, YIN Wen, HU Fa-Long, FAN Hong, FAN Zhi-Long, ZHAO Cai, YU Ai-Zhong, CHAI Qiang. Effect of water and nitrogen reduction on main photosynthetic physiological parameters of film-mulched maize no-tillage rotation wheat [J]. Acta Agronomica Sinica, 2022, 48(2): 437-447.
[14] MA Bo-Wen, LI Qing, CAI Jian, ZHOU Qin, HUANG Mei, DAI Ting-Bo, WANG Xiao, JIANG Dong. Physiological mechanisms of pre-anthesis waterlogging priming on waterlogging stress tolerance under post-anthesis in wheat [J]. Acta Agronomica Sinica, 2022, 48(1): 151-164.
[15] JIAN Hong-Ju, SHANG Li-Na, JIN Zhong-Hui, DING Yi, LI Yan, WANG Ji-Chun, HU Bai-Geng, Vadim Khassanov, LYU Dian-Qiu. Genome-wide identification and characterization of PIF genes and their response to high temperature stress in potato [J]. Acta Agronomica Sinica, 2022, 48(1): 86-98.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
Add: No. 80 Xueyuan South Rd, Beijing 100081, P. R. China E-mail: zwxb301@caas.cn
Supported by Beijing Magtech Co.Ltd