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http://dx.doi.org/10.5423/PPJ.OA.04.2019.0111

Connection the Rhizomicrobiome and Plant MAPK Gene Expression Response to Pathogenic Fusarium oxysporum in Wild and Cultivated Soybean

Chang, Chunling (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
Xu, Shangqi (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
Tian, Lei (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
Shi, Shaohua (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
Nasir, Fahad (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
Chen, Deguo (College of Life Science, Jilin Agricultural University)
Li, Xiujun (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)
Tian, Chunjie (Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences)

Publication Information

The Plant Pathology Journal / v.35, no.6, 2019 , pp. 623-634 More about this Journal

Abstract

Little known the connections between soybeans mitogen-activated protein kinase (MAPK) gene expression and the rhizomicrobiome upon invasion of the root pathogen Fusarium oxysporum. To address this lack of knowledge, we assessed the rhizomicrobiome and root transcriptome sequencing of wild and cultivated soybean during the invasion of F. oxysporum. Results indicated F. oxysporum infection enriched Bradyrhizobium spp. and Glomus spp. and induced the expression of more MAPKs in the wild soybean than cultivated soybean. MAPK gene expression was positively correlated with Pseudomonadaceae but negatively correlated with Sphingomonadaceae and Glomeraceae in both cultivated and wild soybean. Specifically, correlation profiles revealed that Pseudomonadaceae was especially correlated with the induced expression of GmMAKKK13-2 (Glyma.14G195300) and GmMAPK3-2 (Glyma.12G073000) in wild and cultivated soybean during F. oxysporum invasion. Main fungal group Glomeraceae was positively correlated with GmMAPKKK14-1 (Glyma.18G060900) and negatively correlated with GmRaf6-4 (Glyma.02G215300) in the wild soybean response to pathogen infection; while there were positive correlations between Hypocreaceae and GmMAPK3-2 (Glyma.12G073000) and between Glomeraceae and GmRaf49-3 (Glyma.06G055300) in the wild soybean response, these correlations were strongly negative in the response of cultivated soybean to F. oxysporum. Taken together, MAPKs correlated with different rhizomicrobiomes indicating the host plant modulated by the host self-immune systems in response to F. oxysporum.

Keywords

cultivated soybean; Fusarium oxysporum Schltdl.; mitogen-activated protein kinase (MAPK) genes; rhizomicrobiome; wild soybean;

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Reference

1	Abarenkov, K., Henrik Nilsson, R., Larsson, K. H., Alexander, I. J., Eberhardt, U., Erland, S., Hoiland, K., Kjoller, R., Larsson, E., Pennanen, T., Sen, R., Taylor, A. F., Tedersoo, L., Ursing, B. M., Vralstad, T., Liimatainen, K., Peintner, U. and Koljalg, U. 2010. The UNITE database for molecular identification of fungi: recent updates and future perspectives. New Phytol. 186:281-285. DOI
2	Andreasson, E. and Ellis, B. 2010. Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci. 15:106-113. DOI
3	Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W.-L., Gomez-Gomez, L., Boller, T., Ausubel, F. M. and Sheen, J. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983. DOI
4	Bartsev, A. V., Deakin, W. J., Boukli, N. M., McAlvin, C. B., Stacey, G., Malnoe, P., Broughton, W. J. and Staehelin, C. 2004. NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions. Plant Physiol. 134:871-879. DOI
5	Boller, T. and He, S. Y. 2009. Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742-744. DOI
6	Bulgarelli, D., Garrido-Oter, R., Munch, P. C., Weiman, A., Droge, J., Pan, Y., McHardy, A. C. and Schulze-Lefert, P. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392-403. DOI
7	Dean, R., Van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., Di Pietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J. and Foster, G. D. 2012. The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13:414-430. DOI
8	Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., Mc-Donald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Turnbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J. and Knight, R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods. 7:335-336. DOI
9	Chang, C., Tian, L., Ma, L. N., Li, W., Nasir, F., Li, X., Tran, L.-S. P. and Tian, C. 2018. Differential responses of molecular mechanims and physiochemical characters in wild and cultivated soybeans against invasion by the pathogenic Fusarium oxysporum Schltdl. Physiol. Plant. 166:1008-1025. DOI
10	Chisholm, S. T., Coaker, G., Day, B. and Staskawicz, B. J. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-814. DOI
11	DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P. and Andersen, G. L. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069-5072. DOI
12	Dodds, P. N. and Rathjen, J. P. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548. DOI
13	Jimenez, D. R. C. 2017. Soybean root rot caused by Fusarium oxysporum and Fusarium graminearum: interactions with biotic and abiotic factors. Ph.D. thesis. Iowa State University, Ames, IA, USA.
14	Edwards, J., Johnson, C., Santos-Medellin, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., Eisen, J. A. and Sundaresan, V. 2015. Structure, variation, and assembly of the rootassociated microbiomes of rice. Proc. Natl. Acad. Sci. U. S. A. 112:E911-E920. DOI
15	Fernandez-Pascual, M., Lucas, M. M., de Felipe, M. R., Bosca, L., Hirt, H. and Golvano, M. P. 2006. Involvement of mitogenactivated protein kinases in the symbiosis Bradyrhizobium-Lupinus. J. Exp. Bot. 57:2735-2742. DOI
16	Garbeva, P., van Veen, J. A. and van Elsas, J. D. 2004. Microbail diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu. Rev. Phytopathol. 42:243-270. DOI
17	Jimtha, J. C., Smitha, P. V., Anisha, C., Deepthi, T., Meekha, G., Radhakrishnan, E. K., Gayatri, G. P. and Remakanthan, A. 2014. Isolation of endophytic bacteria from embryogenic suspension culture of banana and assessment of their plant growth promoting properties. Plant Cell Tissue Organ Cult. 118:57-66. DOI
18	Kim, M., Hyten, D. L., Niblack, T. L. and Diers, B. W. 2011. Stacking resistance alleles from wild and domestic soybean sources improves soybean cyst nematode resistance. Crop Sci. 51:934-943. DOI
19	Li, G., Zhou, X. and Xu, J.-R. 2012. Genetic control of infectionrelated development in Magnaporthe oryzae. Curr. Opin. Microbiol. 15:678-684. DOI
20	Li, Y., Guan, R., Liu, Z., Ma, Y., Wang, L., Li, L., Lin, F., Luan, W., Chen, P., Yan, Z., Guan, Y., Zhu, L., Ning, X., Smulders, M. J., Li, W., Piao, R., Cui, Y., Yu, Z., Guan, M., Chang, R., Hou, A., Shi, A., Zhang, B., Zhu, S. and Qiu, L. 2008. Genetic structure and diversity of cultivated soybean (Glycine max (L.) Merr.) landraces in China. Theor. Appl. Genet. 117:857-871. DOI
21	Luo, S., Tian, L., Chang, C., Wang, S., Zhang, J., Zhou, X., Li, X., Tran, L.-S. P. and Tian, C. 2018. Grass and maize vegetation systems restore saline-sodic soils in the Songnen Plain of northeast China. Land Degrad. Dev. 29:1107-1119. DOI
22	Liu, Z., Li, Y., Ma, L., Wei, H., Zhang, J., He, X. and Tian, C. 2015. Coordinated regulation of arbuscular mycorrhizal fungi and soybean MAPK pathway genes improved mycorrhizal soybean drought tolerance. Mol. Plant-Microbe Interact. 28:408-419. DOI
23	Louca, S., Parfrey, L. W. and Doebeli, M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science 353:1272-1277. DOI
24	Lundberg, D. S., Lebeis, S. L., Paredes, S. H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., del Rio, T. G., Edgar, R. C., Eickhorst, T., Ley, R. E., Hugenholtz, P., Tringe, S. G. and Dangl, J. L. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488:86-90. DOI
25	Magoc, T. and Salzberg, S. L. 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957-2963. DOI
26	Micallef, S. A., Shiaris, M. P. and Colon-Carmona, A. 2009. Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 60:1729-1742. DOI
27	Peiffer, J. A., Spor, A., Koren, O., Jin, Z., Tringe, S. G., Dangl, J. L., Buckler, E. S. and Ley, R. E. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc. Natl. Acad. Sci. U. S. A. 110:6548-6553. DOI
28	Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H. and Shibuya, N. 2007. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 104:19613-19618. DOI
29	Neupane, A., Nepal, M. P., Piya, S., Subramanian, S., Rohila, J. S., Reese, R. N. and Benson, B. V. 2013. Identification, nomenclature, and evolutionary relationships of mitogen-activated protein kinase (MAPK) genes in soybean. Evol. Bioinform. Online 9:363-386. DOI
30	Ofek-Lalzar, M., Sela, N., Goldman-Voronov, M., Green, S. J., Hadar, Y. and Minz, D. 2013. Niche and host-associated functional signatures of the root surface microbiome. Nat. Commun. 5:4950. DOI
31	Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M. and Bakker, P. A. H. M. 2014. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52:347-375. DOI
32	Pitzschke, A., Schikora, A. and Hirt, H. 2009. MAPK cascade signalling networks in plant defence. Curr. Opin. Plant Biol. 12:421-426. DOI
33	Rodriguez, M. C., Petersen, M. and Mundy, J. 2010. Mitogenactivated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61:621-649. DOI
34	Rosenblueth, M. and Martinez-Romero, E. 2006. Bacterial endophytes and their interactions with hosts. Mol. Plant-Microbe Interact. 19:827-837. DOI
35	Tian, L., Shi, S., Nasir, F., Chang, C., Li, W., Tran, L.-S. P. and Tian, C. 2018. Comparative analysis of the root transcriptomes of cultivated and wild rice varieties in response to Magnaporthe oryzae infection revealed both common and species-specific pathogen responses. Rice 11:26. DOI
36	Scandiani, M. M., Luque, A. G., Razori, M. V., Ciancio Casalini, L., Aoki, T., O'Donnell, K., Cervigni, G. D. L. and Spampinato, C. P. 2015. Metabolic profiles of soybean roots during early stages of Fusarium tucumaniae infection. J. Exp. Bot. 66:391-402. DOI
37	Schoenbeck, M. A., Samac, D. A., Fedorova, M., Gregerson, R. G., Gantt, J. S. and Vance, C. P. 1999. The alfalfa (Medicago sativa) TDY1 gene encodes a mitogen-activated protein kinase homolog. Mol. Plant-Microbe Interact. 12:882-893. DOI
38	Segonzac, C., Feike, D., Gimenez-Ibanez, S., Hann, D. R., Zipfel, C. and Rathjen, J. P. 2011. Hierarchy and roles of pathogenassociated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiol. 156:687-699. DOI
39	Shoresh, M., Gal-On, A., Leibman, D. and Chet, I. 2006. Characterization of a mitogen-activated protein kinase gene from cucumber required for trichoderma-conferred plant resistance. Plant Physiol. 142:1169-1179. DOI
40	Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P.-L. and Ideker, T. 2010. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27:431-432.
41	Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L. and Pachter, L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7:562-578. DOI
42	Tu, J. C. 1987. Integrated control of the pea root rot disease complex in Ontario. Plant Dis. 71:9-13. DOI
43	Zhou, X., Tian, L., Zhang, J., Ma, L., Li, X. and Tian, C. 2017. Rhizospheric fungi and their link with the nitrogen-fixing Frankia harbored in host plant Hippophae rhamnoides L. J. Basic Microbiol. 57:1055-1064. DOI
44	Turra, D., Segorbe, D. and Di Piertro, A. 2014. Protein kinases in plant-pathogenic fungi: conserved regulators of infection. Annu. Rev. Phytopathol. 52:267-288. DOI
45	Weidmann, S., Sanchez, L., Descombin, J., Chatagnier, O., Gianinazzi, S. and Gianinazzi-Pearson, V. 2004. Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol. Plant-Microbe Interact. 17:1385-1393. DOI
46	White, T. J., Bruns, T., Lee, S. and Taylor, J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications, eds. by M. A. Innis, D. H. Gelfand and J. J. Sninsky, pp. 315-322. Academic Press, New York, USA.
47	Zhang, J., Wang, J., Jiang, W., Liu, J., Yang, S., Gai, J. and Li, Y. 2016. Identification and analysis of $NaHCO_3$ stress responsive genes in wild soybean (Glycine soja) roots by RNA-seq. Front. Plant Sci. 7:1842.
48	Zhang, S. and Klessig, D. F. 2001. MAPK cascades in plant defense signaling. Trends Plant Sci. 6:520-527. DOI