绿僵菌mad2敲除株构建及其生物学和诱导植物响应的功能分析

doi:10.3864/j.issn.0578-1752.2021.22.008

Abstract

Abstract:

【Objective】 Metarhizium anisopliae, an entomopathogenic fungus, is found also an endophyte. MAD2 is known to be one of the two adhesin proteins of M. anisopliae, which plays a vital role in adhesion and colonization in plants, but its functional mechanism is poorly understood. The objective of this study is to explore the functional effect of MAD2 protein on the characteristics of growth, virulence, adhesion and inducing plant responses in M. anisopliae by construction of the mad2 mutant strain (Δmad2) of M. anisopliae strain Ma9. 【Method】 The genomic DNA sequences of mad2 anteroposterior were obtained from NCBI, and specific primers were designed to amplify mad2 homologous arm genes S1 and S2 by PCR based on genomic DNA template of M. anisopliae strain Ma9. Meanwhile, Hyg-F/R primer pair was designed to amplify hygromycin gene with promoter sequence based on pKH-KO vector DNA template. Then, homologous knockout boxes S1H and S2H of mad2 were constructed by overlap PCR. Finally, mad2-knockout strains with stable inheritance were obtained by PEG-mediated protoplast transformation of the homologous knockout boxes. By comparing the biological characteristics of the knockout strains (Δmad2) to the wild-type strains (WT), the effects of MAD2 protein on the characteristics of M. anisopliae growth, virulence, adhesion and inducing the peanut response of symbiosis genes were analyzed. 【Result】 Homologous recombination transformants with mad2 knockout were obtained by protoplast transformation. The spore germination rate of Δmad2 was significantly decreased and spore semi-germination time was significantly prolonged 5.47 h compare to WT, as well as the mycelium length of Δmad2 was significantly shorter than WT in 12 h and 14 h incubation, which occupied 77.8% and 76.3% of WT, respectively. The sporulation in 12-day incubation was reduced by 33.3% compared to WT. The ability of Δmad2 strain adhesion in onion was significantly decreased but showed no difference in adhere to the underwings of locust. In addition, mad2-knockout did not affect the virulence of M. anisopliae to silkworm. In the peanut inoculated mad2-knockout strain for 12 h, the transcription level of symbiosis receptor gene SYMRK, calcium signal decoding related genes (CAM, CCaMK, DELLA), lipid and nitrogen transfer related genes (LTP1, NRT24, ABCC2) was significantly down-regulated compared to the treatment of WT. While compared with blank control, Δmad2 still had certainly up-regulated SYMRK transcription level, significantly inhibited the transcription levels of CAM, CCAMK and DELLA, but had no effect on the transcription level of ABCC2, LTP1 and NRT24. 【Conclusion】 M. anisopliae adhesin protein MAD2 affects spore germination, initial growth of mycelium, sporulation quantity and plants adhesion, while has no effect on insect adhesion and virulence of strain, and MAD2 triggers the transcription of peanut symbiotic genes at the initial stage of interaction between the strain and peanut.

Key words: Metarhizium anisopliae, adhesin protein MAD2, gene knockout, adhesion, virulence, growth trait

CAI Ni,YAN DuoZi,NONG XiangQun,WANG GuangJun,TU XiongBing,ZHANG ZeHua. Adhesin Gene mad2 Knockout and Functional Effects on Biological Characteristics and Inducing Plant Responses in Metarhizium anisopliae[J].Scientia Agricultura Sinica, 2021, 54(22): 4800-4812.

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References 41

[1]	MENG Y, ZHANG X, GUO N, FANG W. Mrst12 implicated in the regulation of transcription factor AFTF1 by Fus3-MAPK during cuticle penetration by the entomopathogenic fungus Metarhizium robertsii. Fungal Genetics and Biology, 2019, 131: 103244. DOI: 10.1016/j.fgb.2019.103244. doi: 10.1016/j.fgb.2019.103244
[2]	PARSA S, ORTIZ V, GÓMEZ-JIMÉNEZ M I, KRAMER M, VEGA F E. Root environment is a key determinant of fungal entomopathogen endophytism following seed treatment in the common bean, Phaseolus vulgaris. Biological Control, 2018, 116: 74-81. DOI: 10.1016/j.biocontrol.2016.09.001. doi: 10.1016/j.biocontrol.2016.09.001
[3]	STEINWENDER B M, ENKERLI J, WIDMER F, EILENBERG J, KRISTENSEN H L, BIDOCHKA M J, MEYLING N V. Root isolations of Metarhizium spp. from crops reflect diversity in the soil and indicate no plant specificity. Journal of Invertebrate Pathology, 2015, 132: 142-148. DOI: 10.1016/j.jip.2015.09.007. doi: 10.1016/j.jip.2015.09.007
[4]	RAYA-DÍAZ S, SÁNCHEZ-RODRÍGUEZ A R, SEGURA-FERNÁNDEZ J M, DEL CARMEN DEL CAMPILLO M, QUESADA-MORAGA E. Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates. PLoS ONE, 2017, 12(10): e0185903. DOI: 10.1371/journal.pone.0185903. doi: 10.1371/journal.pone.0185903
[5]	KHAN A L, HAMAYUN M, KANG S M, KIM Y H, JUNG H Y, LEE J H, LEE I J. Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: An example of Paecilomyces formosus LHL10. BMC Microbiology, 2012, 12: 3. DOI: 10.1186/1471-2180-12-3. doi: 10.1186/1471-2180-12-3
[6]	AKELLO J, SIKORA R. Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biological Control, 2012, 61(3): 215-221. DOI: 10.1016/j.biocontrol.2012.02.007. doi: 10.1016/j.biocontrol.2012.02.007
[7]	WANG C, ST LEGER R J. The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryotic Cell, 2007, 6(5): 808-816. DOI: 10.1128/EC.00409-06. doi: 10.1128/EC.00409-06
[8]	NICHOLSON R L, EPSTEIN L. Adhesion of fungi to the plant surface// COLE G T. The Fungal Spore and Disease Initiation in Plants and Animals. Springer US, 1991: 3-23. DOI: https://doi.org/10.1007/978-1-4899-2635-7_1. doi: https://doi.org/10.1007/978-1-4899-2635-7_1
[9]	SHEPPARD D C, YEAMAN M R, WELCH W H, PHAN Q T, FU Y, IBRAHIM A S, FILLER S G, ZHANG M, WARING A J, JR EDWARDS J E. Functional and structural diversity in the Als protein family of Candida albicans. The Journal of Biological Chemistry, 2004, 279(29): 30480-30489. DOI: 10.1074/jbc.M401929200. doi: 10.1074/jbc.M401929200
[10]	PAVA-RIPOLL M, ANGELINI C, FANG W, WANG S, POSADA F J, ST LEGER R. The rhizosphere-competent entomopathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudate. Microbiology, 2011, 157(1): 47-55. DOI: 10.1099/mic.0.042200-0. doi: 10.1099/mic.0.042200-0
[11]	闫多子, 蔡霓, 王峰, 农向群, 王广君, 涂雄兵, 张泽华. 绿僵菌黏附素MAD1体外表达及诱导花生响应的作用. 中国农业科学, 2021, 54(4): 744-753. DOI: 10.3864/j.issn.0578-1752.2021.04.007. doi: 10.3864/j.issn.0578-1752.2021.04.007
	YAN D Z, CAI N, WANG F, NONG X Q, WANG G J, TU X B, ZHANG Z H. Expression in vitro of Metarhizium anisopliae adhesin MAD1 and its effect on inducing response in peanut. Scientia Agricultura Sinica, 2021, 54(4): 744-753. DOI: 10.3864/j.issn.0578-1752.2021.04.007. (in Chinese) doi: 10.3864/j.issn.0578-1752.2021.04.007
[12]	KRELL V, UNGER S, JAKOBS-SCHÖNWANDT D, PATEL A V. Endophytic Metarhizium brunneum mitigates nutrient deficits in potato and improves plant productivity and vitality. Fungal Ecology, 2018, 34: 43-49. DOI: 10.1016/j.funeco.2018.04.002. doi: 10.1016/j.funeco.2018.04.002
[13]	BEHIE S W, BIDOCHKA M J. Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: An additional branch of the soil nitrogen cycle. Applied and Environmental Microbiology, 2014, 80(5): 1553-1560. DOI: 10.1128/AEM.03338-13. doi: 10.1128/AEM.03338-13
[14]	BEHIE S W, MOREIRA C C, SEMENTCHOUKOVA I, BARELLI L, ZELISKO P M, BIDOCHKA M J. Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nature Communications, 2017, 8: 14245. DOI: 10.1038/ncomms14245. doi: 10.1038/ncomms14245
[15]	BEHIE S W, ZELISKO P M, BIDOCHKA M J. Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science, 2012, 336(6088): 1576-1577. DOI: 10.1126/science.1222289. doi: 10.1126/science.1222289
[16]	SASAN R K, BIDOCHKA M J. The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. American Journal of Botany, 2012, 99(1): 101-107. DOI: 10.3732/ajb.1100136. doi: 10.3732/ajb.1100136
[17]	LIAO X, O’BRIEN T R, FANG W, ST LEGER R J. The plant beneficial effects of Metarhizium species correlate with their association with roots. Applied Microbiology and Biotechnology, 2014, 98(16): 7089-7096. DOI: 10.1007/s00253-014-5788-2. doi: 10.1007/s00253-014-5788-2
[18]	BEHIE S W, JONES S J, BIDOCHKA M J. Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology, 2015, 13: 112-119. DOI: 10.1016/j.funeco.2014.08.001. doi: 10.1016/j.funeco.2014.08.001
[19]	CAI N, WANG F, NONG X Q, WANG G J, MCNEILL M, CAO G C, HAO K, LIU S F, ZHANG Z H. Visualising confirmation of the endophytic relationship of Metarhizium anisopliae with maize roots using molecular tools and fluorescent labelling. Biocontrol Science and Technology, 2019, 29(11): 1023-1036. DOI: 10.1080/09583157.2019.1641792. doi: 10.1080/09583157.2019.1641792
[20]	HAO K, WANG F, NONG X Q, MCNEILL M R, LIU S F, WANG G J, CAO G C, ZHANG Z H. Response of peanut Arachis hypogaea roots to the presence of beneficial and pathogenic fungi by transcriptome analysis. Scientific Reports, 2017, 7(1): 964. DOI: 10.1038/s41598-017-01029-3. doi: 10.1038/s41598-017-01029-3
[21]	徐芳, 姚泉洪, 熊爱生, 彭日荷, 侯喜林, 曹兵. 重叠延伸PCR技术及其在基因工程上的应用. 分子植物育种, 2006, 4(5): 747-750. DOI: 10.3969/j.issn.1672-416X.2006.05.025. doi: 10.3969/j.issn.1672-416X.2006.05.025
	XU F, YAO Q H, XIONG A S, PENG R H, HOU X L, CAO B. SOE PCR and its application in genetic engineering. Molecular Plant Breeding, 2006, 4(5): 747-750. DOI: 10.3969/j.issn.1672-416X.2006.05.025. (in Chinese) doi: 10.3969/j.issn.1672-416X.2006.05.025
[22]	王晓玲, 蒋伶活, 张泽华. 以G418抗性为选择标记的金龟子绿僵菌原生质体转化的研究. 安徽农业科学, 2007, 35(28): 8865-8866, 8868. DOI: 10.3969/j.issn.0517-6611.2007.28.020. doi: 10.3969/j.issn.0517-6611.2007.28.020
	WANG X L, JIANG L H, ZHANG Z H. Protoplast transformation of Metarhizium anisopliae with G418 resistance as selective marker. Journal of Anhui Agricultural Sciences, 2007, 35(28): 8865-8866, 8868. DOI: 10.3969/j.issn.0517-6611.2007.28.020. (in Chinese) doi: 10.3969/j.issn.0517-6611.2007.28.020
[23]	刘艳微. 转Mad1基因球孢白僵菌工程菌株的构建及鉴定[D]. 哈尔滨: 哈尔滨师范大学, 2015. DOI: 10.7666/d.D678481. doi: 10.7666/d.D678481
	LIU Y W. Construction and identification of Mad1 transgenic Beauveria bassiana strains[D]. Harbin: Harbin Normal University, 2015. DOI: 10.7666/d.D678481. (in Chinese) doi: 10.7666/d.D678481
[24]	蔡守平, 何学友, 曾丽琼, 黄金水, 钟景辉, 嵇保中. 感染星天牛幼虫高致病力金龟子绿僵菌菌株的筛选. 中国生物防治学报, 2012, 28(2): 293-297. DOI: 10.3969/j.issn.2095-039X.2012.02.023. doi: 10.3969/j.issn.2095-039X.2012.02.023
	CAI S P, HE X Y, ZENG L Q, HUANG J S, ZHONG J H, JI B Z. Susceptibility of Anoplophora chinensis larvae to the entomopathogenic fungus, Metarhzium anisopliae. Chinese Journal of Biological Control, 2012, 28(2): 293-297. DOI: 10.3969/j.issn.2095-039X.2012.02.023. (in Chinese) doi: 10.3969/j.issn.2095-039X.2012.02.023
[25]	MAYO S, COMINELLI E, SPARVOLI F, GONZÁLEZ-LÓPEZ O, RODRÍGUEZ-GONZÁLEZ A, GUTIÉRREZ S, CASQUERO P A. Development of a qPCR strategy to select bean genes involved in plant defense response and regulated by the Trichoderma velutinum - Rhizoctonia solani interaction. Frontiers in Plant Science, 2016, 7: 1109. DOI: 10.3389/fpls.2016.01109. doi: 10.3389/fpls.2016.01109
[26]	廉翠红, 刘维达. 与白念珠菌黏附和侵入相关的毒力因子研究进展. 国际皮肤性病学杂志, 2004, 30(5): 323-325. DOI: 10.3760/cma.j.issn.1673-4173.2004.05.018. doi: 10.3760/cma.j.issn.1673-4173.2004.05.018
	LIAN C H, LIU W D. Research progress on virulence factors related to adhesion and invasion of Candida albicans. International Journal of Dermatology and Venereology, 2004, 30(5): 323-325. DOI: 10.3760/cma.j.issn.1673-4173.2004.05.018. (in Chinese) doi: 10.3760/cma.j.issn.1673-4173.2004.05.018
[27]	WÄCHTLER B, CITIULO F, JABLONOWSKI N, FÖRSTER S, DALLE F, SCHALLER M, WILSON D, HUBE B. Candida albicans-epithelial interactions: Dissecting the roles of active penetration, induced endocytosis and host factors on the infection process. PLoS ONE, 2012, 7(5): e36952. DOI: 10.1371/journal.pone.0036952. doi: 10.1371/journal.pone.0036952
[28]	SILVERMAN R J, NOBBS A H, VICKERMAN M M, BARBOUR M E, JENKINSON H F. Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infection and Immunity, 2010, 78(11): 4644-4652. DOI: 10.1128/IAI.00685-10. doi: 10.1128/IAI.00685-10
[29]	MURCIANO C A, MOYES D L, RUNGLALL M, TOBOUTI P, ISLAM A, HOYER L L, NAGLIK J R. Evaluation of the role of Candida albicans agglutinin-like sequence (Als) proteins in human oral epithelial cell interactions. PLoS ONE, 2012, 7(3): e33362. DOI: 10.1371/journal.pone.0033362. doi: 10.1371/journal.pone.0033362
[30]	STAAB J F, BRADWAY S D, FIDEL P L, SUNDSTROM P. Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science, 1999, 283(5407): 1535-1538. DOI: 10.1126/science.283.5407.1535. doi: 10.1126/science.283.5407.1535
[31]	GALE C A, BENDEL C M, MCCLELLAN M, HAUSER M, BECKER J M, BERMAN J, HOSTETTER M K. Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1. Science, 1998, 279(5355): 1355-1358. DOI: 10.1126/science.279.5355.1355. doi: 10.1126/science.279.5355.1355
[32]	FU Y, IBRAHIM A S, SHEPPARD D C, CHEN Y C, FRENCH S W, CUTLER J E, FILLER S G, EDWARDS J E. Candida albicans ALS1p: An adhesin that is a downstream effector of the EFG1 filamentation pathway. Molecular Microbiology, 2002, 44(1): 61-72. DOI: 10.1046/j.1365-2958.2002.02873.x. doi: 10.1046/j.1365-2958.2002.02873.x
[33]	BARELLI L, PADILLA-GUERRERO I E, BIDOCHKA M J. Differential expression of insect and plant specific adhesin genes, Mad1 and Mad2, in Metarhizium robertsii. Fungal Biology, 2011, 115(11): 1174-1185. DOI: 10.1016/j.funbio.2011.08.003. doi: 10.1016/j.funbio.2011.08.003
[34]	BATISTI O, KUDLA J. Analysis of calcium signaling pathways in plants. Biochimica et Biophysica Acta, 2012, 1820(8): 1283-1293. DOI: 10.1016/j.bbagen.2011.10.012. doi: 10.1016/j.bbagen.2011.10.012
[35]	熊珊珊, 赵斌. 丛枝菌根真菌的钙调素基因在共生过程中的作用. 湖北农业科学, 2014, 53(13): 3177-3182. DOI: 10.3969/j.issn.0439-8114.2014.13.052. doi: 10.3969/j.issn.0439-8114.2014.13.052
	XIONG S S, ZHAO B. The roles of calmodulin gene of Glomus intraradices in symbiosis process. Hubei Agricultural Sciences, 2014, 53(13): 3177-3182. DOI: 10.3969/j.issn.0439-8114.2014.13.052. (in Chinese) doi: 10.3969/j.issn.0439-8114.2014.13.052
[36]	MACLEAN A M, BRAVO A, HARRISON M J. Plant signaling and metabolic pathways enabling arbuscular mycorrhizal symbiosis. The Plant Cell, 2017, 29(10): 2319-2335. DOI: 10.1105/tpc.17.00555. doi: 10.1105/tpc.17.00555
[37]	WANG F, NONG X Q, HAO K, CAI N, WANG G J, LIU S F, ULLAH H, ZHANG Z H. Identification of the key genes involved in the regulation of symbiotic pathways induced by Metarhizium anisopliae in peanut (Arachis hypogaea) roots. 3 Biotech, 2020, 10(3): 124. DOI: 10.1007/s13205-020-2105-x. doi: 10.1007/s13205-020-2105-x
[38]	JIN Y, LIU H, LUO D, YU N, DONG W, WANG C, ZHANG X, DAI H, YANG J, WANG E. Della proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nature Communications, 2016, 7: 12433. DOI: 10.1038/ncomms12433. doi: 10.1038/ncomms12433
[39]	邵若玄, 沈忆珂, 周文彬, 方佳, 郑炳松. 植物ATP结合盒(ABC)转运蛋白研究进展. 浙江农林大学学报, 2013, 30(5): 761-768. DOI: 10.11833/j.issn.2095-0756.2013.05.020. doi: 10.11833/j.issn.2095-0756.2013.05.020
	SHAO R X, SHEN Y K, ZHOU W B, FANG J, ZHENG B S. Recent advances for plant ATP-binding cassette transporters. Journal of Zhejiang A&F University, 2013, 30(5): 761-768. DOI: 10.11833/j.issn.2095-0756.2013.05.020. (in Chinese) doi: 10.11833/j.issn.2095-0756.2013.05.020
[40]	CARVALHO A O, GOMES V M. Role of plant lipid transfer proteins in plant cell physiology: A concise review. Peptides, 2007, 28: 1144-1153. DOI: 10.1016/j.peptides.2007.03.004. doi: 10.1016/j.peptides.2007.03.004
[41]	李国纪, 朱林, 曹金山, 王幼宁. 大豆GmNRT1.2a和GmNRT1.2b基因的克隆及功能探究. 作物学报, 2020, 46(7): 1025-1032. DOI: 10.3724/SP.J.1006.2020.94152. doi: 10.3724/SP.J.1006.2020.94152
	LI G J, ZHU L, CAO J S, WANG Y N. Cloning and functional analysis of GmNRT1.2a and GmNRT1.2b in soybean. Acta Agronomica Sinica, 2020, 46(7): 1025-1032. DOI: 10.3724/SP.J.1006.2020.94152. (in Chinese) doi: 10.3724/SP.J.1006.2020.94152

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引物名称Primer name	序列Sequence	片段长度Sequence length (bp)
Hyg-F	5′-ATGCCTCAGCGAATTCGATAACTG-3′	1426
Hyg-R	5′-GTTCCCGGTCGGCATCTACTCTA-3′	1426
mad2 S1-F	5′-CCCATTGTCTC CACGCACACT-3′	1046
mad2 S1-R	5′-GTTATCGAATTCGCTGAGGCATCGAAGGTATAAGGTGAGAGCGGTTG-3′	1046
mad2 S2-F	5′-TAGAGTAGATGCCGACCGGGAACGTTGACCGCACAGCATAT ATCCTGG-3′	1174
mad2 S2-R	5′-CCCAGCAACAAGCCCACATGCAGCAA-3′	1174
Hyg S2-F	5′-CAGCTTCGATGTAGGAGGGCGTGG-3′	1174 + 936
Hyg S1-R	5′-GGCAGTCCTCGGCCCAAAGCATCAG-3′	1046 + 945
OUT-mad2-F	5′-ATGAAGTCTTTCATTGCTGTTGCGG-3′	921
OUT-mad2-R	5′-CTAGATCAGGAGAGCGGCGATGAGG-3′	921

基因Gene	引物序列Primer sequence	基因Gene	引物序列Primer sequence
RPL7	5′-ACAGTTGGTCCTCACTTCAG-3′	LTP1	5′-CAACCAACCAATCACCCTC-3′
RPL7	5′-GCTCATTTATGTAAGCTTCCCT-3′	LTP1	5′-GGGCTAATCTTGTATGGGATG-3′
CCaMK	5′-ATCCGCCTTTCATTGCTC-3′	NRT24	5′-CCCACGGAGAAGAGAATCATC-3′
CCaMK	5′-GAACATCTTTGGCTACATCACC-3′	NRT24	5′-GGAATGGCAAACATCATAGCAC-3′
ABCC2	5′-CTCATAGGCATTGTCAGCAC-3′	DELLA	5′-CCTCCACCATCACAACTTCC-3′
ABCC2	5′-GTGAATCGGATGTTGTTGTC-3′	DELLA	5′-CATTCTCCTGCGAGTCAACC-3′
SYMRK	5′-AAGCAATGTGGAGAGTGGTG-3′	CaM	5′-TGATGGCTAAGTGAGGACC-3′
SYMRK	5′-AGATGAAGTAGAGGGCGGAA-3′	CaM	5′-AATGAAAGCAAGGGACAGAG-3′

Adhesin Gene mad2 Knockout and Functional Effects on Biological Characteristics and Inducing Plant Responses in Metarhizium anisopliae

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