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Research Article | Open Access

miR398b negatively regulates cotton immune responses to Verticillium dahliae via multiple targets

Yuhuan Miaoa,b, Kun Chena, Jinwu Dengc, Lin Zhanga, Weiran Wangd, Jie Kongd, Steven J. Klostermane, Xianlong Zhanga, Alifu Aierxid( ), Longfu Zhua( )
National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan 430070, Hubei, China
Hubei University of Chinese Medicine, Wuhan 430065, Hubei, China
Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Wuhan 430062, Hubei, China
Institute of Economic Crops, Xinjiang Academy of Agricultural Sciences, Urumchi 842000, Xinjiang, China
United States Department of Agriculture, Agricultural Research Service, Salinas, CA 93905, USA
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Abstract

MicroRNAs (miRNAs) play essential roles in plant defense responses, although such roles have not been identified in cotton in response to the plant pathogenic fungus Verticillium dahliae. In this study, the functions of miR398b and its target genes in cotton-V. dahliae interaction were investigated. The transcript levels of miR398b were down-regulated by V. dahliae infection and miR398b overexpression in cotton made the plants more susceptible to V. dahliae. The results suggest that miR398b negatively regulates cotton resistance to V. dahliae. This may occur by miR398b repression of some CC-NBS-LRR genes via translational inhibition, interfering with defense responses and leading to cotton susceptibility to V. dahliae. Alternatively, miR398b may guide the cleavage of the mRNAs of GhCSD1, GhCSD2 and GhCCS, each of which functions in reactive oxygen species (ROS) regulation and homeostasis, thereby causing excessive ROS accumulation in miR398b-overexpressing plants in response to V. dahliae infection. This study suggests conserved and novel roles of miR398b in the cotton–V. dahliae interaction. These discoveries may be coupled with new strategies in cotton breeding programs to improve resistance to V. dahliae.

Keywords

CottonmiR398bNBS-LRRROS homeostasis Verticillium dahliae

References

[1]

L. Xu, L.F. Zhu, X.L. Zhang, Research on resistance mechanism of cotton to Verticillium wilt, Acta Agron. Sin. 38 (2012) 1553-1560.
Crossref Google Scholar
[2]

D.D. Zhang, J. Wang, D. Wang, Z.Q. Kong, L. Zhou, G.Y. Zhang, Y.J. Gui, J.J. Li, J.Q. Huang, B.L. Wang, C. Liu, C.M. Yin, R.X. Li, T.G. Li, J.L. Wang, D.P.G. Short, S.J. Klosterman, R.M. Bostock, K.V. Subbarao, J.Y. Chen, X.F. Dai, Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae, New Phytol. 222 (2019) 1012-1029.
Crossref Google Scholar
[3]

S.J. Klosterman, Z.K. Atallah, G.E. Vallad, K.V. Subbarao, Diversity, pathogenicity, and management of Verticillium species, Annu. Rev. Phytopathol. 47 (2009) 39-62.
Crossref Google Scholar
[4]

S.T. Chisholm, G. Coaker, B. Day, B.J. Staskawicz, Host-microbe interactions: shaping the evolution of the plant immune response, Cell 124 (2006) 803-814.
Crossref Google Scholar
[5]

J.D.G. Jones, J.L. Dangl, The plant immune system, Nature 444 (2006) 323-329.
Crossref Google Scholar
[6]

E.A. van der Biezen, J.D.G. Jones, The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals, Curr. Biol. 8 (1998) 226-228.
Crossref Google Scholar
[7]

D. Tian, M.B. Traw, J.Q. Chen, M. Kreitman, J. Bergelson, Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana, Nature 423 (2003) 74.
Crossref Google Scholar
[8]

R. Mittler, S. Vanderauwera, N. Suzuki, G. Miller, V.B. Tognetti, K. Vandepoele, M. Gollery, V. Shulaev, F. van Breusegem, ROS signaling: the new wave? Trends Plant Sci. 16 (2011) 300-309.
Crossref Google Scholar
[9]

R. Mittler, ROS are good, Trends Plant Sci. 22 (2017) 11-19.
Crossref Google Scholar
[10]

K. Apel, H. Hirt, Reactive oxygeb species: metabolism, oxidative stress, and signal transduction, Annu. Rev. Plant Biol. 55 (2004) 373-399.
Crossref Google Scholar
[11]

Q. Guan, X. Lu, H. Zeng, Y. Zhang, J. Zhu, Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis, Plant J. 74 (2013) 840-851.
Crossref Google Scholar
[12]

C.H. Huang, W.Y. Kuo, C. Weiss, T.L. Jinn, Copper chaperone-dependent and - independent activation of three copper-zinc superoxide dismutase homologs localized in different cellular compartments in Arabidopsis, Plant Physiol. 158 (2011) 737–746.
Crossref Google Scholar
[13]

X. Leng, P. Wang, X. Zhu, X. Li, T. Zheng, L. Shangguan, J. Fang, Ectopic expression of CSD1 and CSD2 targeting genes of miR398 in grapevine is associated with oxidative stress tolerance, Funct. Integr. Genomics 17 (2017) 697-710.
Crossref Google Scholar
[14]

R. Sunkar, A. Kapoor, J.K. Zhu, Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance, Plant Cell 18 (2006) 2051–2065.
Crossref Google Scholar
[15]

A.E. Voloudakis, P. Marmey, E. Delannoy, A. Jalloul, C. Martinez, M. Nicole, Molecular cloning and characterization of Gossypium hirsutum superoxide dismutase genes during cotton–Xanthomonas campestris pv. malvacearum interaction, Physiol. Mol. Plant Pathol. 68 (2006) 119-127.
Crossref Google Scholar
[16]

W. Xu, Y. Meng, R.P. Wise, Mla- and Rom1-mediated control of microRNA398 and chloroplast copper/zinc superoxide dismutase regulates cell death in response to the barley powdery mildew fungus, New Phytol. 201 (2014) 1396-1412.
Crossref Google Scholar
[17]

B.J. Reinhart, F.J. Slack, M. Basson, A.E. Pasquinelli, J.C. Bettinger, A.E. Rougvie, H.R. Horvitz, G. Ruvkun, The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans, Nature 403 (2000) 901.
Crossref Google Scholar
[18]

B.J. Reinhart, E.G. Weinstein, M.W. Rhoades, B. Bartel, D.P. Bartel, MicroRNAs in plants, Genes Dev. 16 (2002) 1616-1626.
Crossref Google Scholar
[19]

O. Voinnet, Origin, biogenesis, and activity of plant microRNAs, Cell 136 (2009) 669-687.
Crossref Google Scholar
[20]

M. Xie, S. Zhang, B. Yu, microRNA biogenesis, degradation and activity in plants, Cell. Mol. Life Sci. 72 (2015) 87-99.
Crossref Google Scholar
[21]

N.G. Bologna, O. Voinnet, The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis, Annu. Rev. Plant Biol. 65 (2014) 473-503.
Crossref Google Scholar
[22]

J.M. Couzigou, J.P. Combier, Plant microRNAs: key regulators of root architecture and biotic interactions, New Phytol. 212 (2016) 22-35.
Crossref Google Scholar
[23]

C. Guo, Y. Xu, M. Shi, Y. Lai, X. Wu, H. Wang, Z. Zhu, R.S. Poethig, G. Wu, Repression of miR156 by miR159 regulates the timing of the juvenile-to-adult transition in Arabidopsis, Plant Cell 29 (2017) 1293.
Crossref Google Scholar
[24]

W. Huang, S. Peng, Z. Xian, D. Lin, G. Hu, L.u. Yang, M. Ren, Z. Li, Overexpression of a tomato miR171 target gene SlGRAS24 impacts multiple agronomical traits via regulating gibberellin and auxin homeostasis, Plant Biotechnol. J. 15 (2017) 472-488.
Crossref Google Scholar
[25]

H. Zhang, J. Zhang, J. Yan, F. Gou, Y. Mao, G. Tang, J.R. Botella, J.K. Zhu, Short tandem target mimic rice lines uncover functions of miRNAs in regulating important agronomic traits, Proc. Nat. Acad. Sci. U. S. A. 114 (2017) 5277-5282.
Crossref Google Scholar
[26]

Y. Deng, J. Wang, J. Tung, D. Liu, Y. Zhou, S. He, Y. Du, B. Baker, F. Li, S.P. Dinesh-Kumar, A role for small RNA in regulating innate immunity during plant growth, PLoS Pathog. 14 (2018) e1006756.
Crossref Google Scholar
[27]

Y. Ding, Y. Ma, N. Liu, J. Xu, Q. Hu, Y. Li, Y. Wu, S. Xie, L. Zhu, L. Min, X. Zhang, microRNAs involved in auxin signalling modulate male sterility under high-temperature stress in cotton (Gossypium hirsutum), Plant J. 91 (2017) 977-994.
Crossref Google Scholar
[28]

S. Li, C. Castillo-Gonzalez, B. Yu, X. Zhang, The functions of plant small RNAs in development and in stress responses, Plant J. 90 (2017) 654-670.
Crossref Google Scholar
[29]

F. Li, D. Pignatta, C. Bendix, J.O. Brunkard, M.M. Cohn, J. Tung, H. Sun, P. Kumar, B. Baker, MicroRNA regulation of plant innate immune receptors, Proc. Nat. Acad. Sci. U. S. A. 109 (2012) 1790-1795.
Crossref Google Scholar
[30]

P.V. Shivaprasad, H.M. Chen, K. Patel, D.M. Bond, B.A.C.M. Santos, D.C. Baulcombe, A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs, Plant Cell 24 (2012) 859-874.
Crossref Google Scholar
[31]

J. Liu, X. Cheng, D.A. Liu, W. Xu, R. Wise, Q.H. Shen, J.M. McDowell, The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling, PLoS Genet. 10 (2014) e1004755.
Crossref Google Scholar
[32]

C. Cui, J.J. Wang, J.H. Zhao, Y.Y. Fang, X.F. He, H.S. Guo, C.G. Duan, A Brassica miRNA regulates plant growth and immunity through distinct modes of action, Mol. Plant 13 (2020) 231-245.
Crossref Google Scholar
[33]

Q. Fei, Y.U. Zhang, R. Xia, B.C. Meyers, Small RNAs add zing to the Zig-Zag-Zig model of plant defenses, MPMI 29 (2016) 165-169.
Crossref Google Scholar
[34]

Q. Wang, N. Liu, X. Yang, L. Tu, X. Zhang, Small RNA-mediated responses to low- and high-temperature stresses in cotton, Sci. Rep. 6 (2016) 35558.
Crossref Google Scholar
[35]

C. Zhu, Y. Ding, H. Liu, MiR398 and plant stress responses, Physiol. Plant. 143 (2011) 1-9.
Crossref Google Scholar
[36]

G. Jagadeeswaran, A. Saini, R. Sunkar, Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis, Planta 229 (2009) 1009-1014.
Crossref Google Scholar
[37]

Y. Li, Q. Zhang, J. Zhang, L. Wu, Y. Qi, J.M. Zhou, Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity, Plant Physiol. 152 (2010) 2222-2231.
Crossref Google Scholar
[38]

L. Beauclair, A. Yu, N. Bouché, microRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis, Plant J. 62 (2010) 454-462.
Crossref Google Scholar
[39]

M.W. Jones-Rhoades, D.P. Bartel, Computational identification of plant microRNAs and their targets, including a stress-induced miRNA, Mol. Cell 14 (2004) 787-799.
Crossref Google Scholar
[40]

M.D. Curtis, U. Grossniklaus, A gateway cloning vector set for high-throughput functional analysis of genes in planta, Plant Physiol. 133 (2003) 462–469.
Crossref Google Scholar
[41]

Y. Li, X.L. Cao, Y. Zhu, X.M. Yang, K.N. Zhang, Z.Y. Xiao, H.E. Wang, J.H. Zhao, L.L. Zhang, G.B. Li, Y.P. Zheng, J. Fan, J. Wang, X.Q. Chen, X.J. Wu, J.Q. Zhao, O.X. Dong, X.W. Chen, M. Chern, W.M. Wang, Osa-miR398b boosts H2O2 production and rice blast disease-resistance via multiple superoxide dismutases, New Phytol. 222 (2019) 1507-1522.
Crossref Google Scholar
[42]

W. Gao, L.U. Long, L.F. Zhu, L.I. Xu, W.H. Gao, L.Q. Sun, L.L. Liu, X.L. Zhang, Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae, Mol. Cell. Proteomics 12 (2013) 3690-3703.
Crossref Google Scholar
[43]

N. Liu, L. Tu, W. Tang, W. Gao, K. Lindsey, X. Zhang, Small RNA and degradome profiling reveals a role for miRNAs and their targets in the developing fibers of Gossypium barbadense, Plant J. 80 (2014) 331-344.
Crossref Google Scholar
[44]

S. Jin, X. Zhang, Y. Nie, X. Guo, S. Liang, H. Zhu, Identification of a novel elite genotype for in vitro culture and genetic transformation of cotton, Biol. Plant. 50 (2006) 519-524.
Crossref Google Scholar
[45]

L. Sun, L. Zhu, L. Xu, D. Yuan, L. Min, X. Zhang, Cotton cytochrome P450 CYP82D regulates systemic cell death by modulating the octadecanoid pathway, Nat. Commun. 5 (2014) 5372.
Crossref Google Scholar
[46]

R.P. Hellens, A.C. Allan, E.N. Friel, K. Bolitho, K. Grafton, M.D. Templeton, S. Karunairetnam, A.P. Gleave, W.A. Laing, Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants, Plant Methods 1 (2005) 13.
Crossref Google Scholar
[47]

H. Chen, Y. Zou, Y. Shang, H. Lin, Y. Wang, R. Cai, X. Tang, J.M. Zhou, Firefly luciferase complementation imaging assay for protein-protein interactions in plants, Plant Physiol. 146 (2008) 368-376.
Crossref Google Scholar
[48]

W. Gao, L.U. Long, L.I. Xu, K. Lindsey, X. Zhang, L. Zhu, Suppression of the homeobox gene HDTF1 enhances resistance to Verticillium dahliae and Botrytis cinerea in cotton, J. Integr. Plant Biol. 58 (2016) 503-513.
Crossref Google Scholar
[49]

L. Xu, W. Zhang, X. He, M. Liu, K. Zhang, M. Shaban, L. Sun, J. Zhu, Y. Luo, D. Yuan, X. Zhang, L. Zhu, Functional characterization of cotton genes responsive to Verticillium dahliae through bioinformatics and reverse genetics strategies, J. Exp. Bot. 65 (2014) 6679-6692.
Crossref Google Scholar
[50]

R.A. Jefferson, T.A. Kavanagh, M.W. Bevan, GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants, EMBO J. 6 (1987) 3901-3907.
Crossref Google Scholar
[51]

X. Dai, Z. Zhuang, P.X. Zhao, psRNATarget: a plant small RNA target analysis server, Nucleic Acids Res. 46 (2018) 49-54.
Crossref Google Scholar
[52]

Y.H. Miao, L. Xu, X. He, L. Zhang, M. Shaban, X.L. Zhang, L.F. Zhu, Suppression of tryptophan synthase activates cotton immunity by triggering cell death via promoting SA synthesis, Plant J. 98 (2019) 329-345.
Crossref Google Scholar
[53]

Q. Hu, L. Zhu, X. Zhang, Q. Guan, S. Xiao, L. Min, X. Zhang, GhCPK33 negatively regulates defense against Verticillium dahliae by phosphorylating GhOPR3, Plant Physiol. 178 (2018) 876-889.
Crossref Google Scholar
[54]

C. Ottmann, B. Luberacki, I. Kufner, W. Koch, F. Brunner, M. Weyand, L. Mattinen, M. Pirhonen, G. Anderluh, H.U. Seitz, T. Nurnberger, C. Oecking, A common toxin fold mediates microbial attack and plant defense, Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 10359-10364.
Crossref Google Scholar
[55]

D. Qutob, B. Kemmerling, F. Brunner, I. Kufner, S. Engelhardt, A.A. Gust, B. Luberacki, H.U. Seitz, D. Stahl, T. Rauhut, E. Glawischnig, G. Schween, B. Lacombe, N. Watanabe, E. Lam, R. Schlichting, D. Scheel, K. Nau, G. Dodt, D. Hubert, M. Gijzen, T. Nurnberger, Phytotoxicity and innate immune responses induced by Nep1-like proteins, Plant Cell 18 (2006) 3721–3744.

Crossref Google Scholar
[56]

J.Y. Wang, Y.U. Cai, J.Y. Gou, Y.B. Mao, Y.H. Xu, W.H. Jiang, X.Y. Chen, VdNEP, an elicitor from Verticillium dahliae, induces cotton plant wilting, Appl. Environ. Microbiol. 70 (2004) 4989-4995.
Crossref Google Scholar
[57]

X. He, Q. Sun, H. Jiang, X. Zhu, J. Mo, L. Long, L. Xiang, Y. Xie, Y. Shi, Y. Yuan, Y. Cai, Identification of novel microRNAs in the Verticillium wilt-resistant upland cotton variety KV-1 by high-throughput sequencing, SpringerPlus 3 (2014) 564.
Crossref Google Scholar
[58]

G. Hu, M. Hao, L.E. Wang, J. Liu, Z. Zhang, Y.E. Tang, Q. Peng, Z. Yang, J. Wu, The cotton miR477-CBP60A module participates in plant defense against Verticillium dahlia, Mol. Plant-Microbe Interact. 33 (2020) 624-636.
Crossref Google Scholar
[59]

Z. Yin, Y. Li, X. Han, F. Shen, J.H. Ahn, Genome-wide profiling of miRNAs and other small non-coding RNAs in the Verticillium dahliae–inoculated cotton roots, PLoS ONE 7 (2012) e35765.
Crossref Google Scholar
[60]

Q.H. Zhu, L. Fan, Y. Liu, H. Xu, D. Llewellyn, I. Wilson, J. Zhang, miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton, PLoS ONE 8 (2013) e84390.
Crossref Google Scholar
[61]

T. Zhang, Y.L. Zhao, J.H. Zhao, S. Wang, Y. Jin, Z.Q. Chen, Y.Y. Fang, C.L. Hua, S.W. Ding, H.S. Guo, Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen, Nat. Plants 2 (2016) 1-6.
Crossref Google Scholar
[62]

P. Brodersen, L. Sakvarelidze-Achard, M. Bruun-Rasmussen, P. Dunoyer, Y.Y. Yamamoto, L. Sieburth, O. Voinnet, Widespread translational inhibition by plant miRNAs and siRNAs, Science 320 (2008) 1185-1190.
Crossref Google Scholar
[63]
X. Chen, O. Rechavi, Plant and animal small RNA communications between cells and organisms, Nat. Rev. Mol. Cell Biol. (2021), https://doi.org/10.1038/s41580-021-00425-y.
Crossref
[64]

J.J. Song, S.K. Smith, G.J. Hannon, L. Joshua-Tor, Crystal structure of Argonaute and its implications for RISC slicer activity, Science 305 (2004) 1434-1437.
Crossref Google Scholar
[65]

Y.L. Zhao, T.T. Zhou, H.S. Guo, R.A. Wilson, Hyphopodium-specific VdNoxB/VdPls1-dependent ROS-Ca2+ signaling is required for plant infection by Verticillium dahliae, PLoS Pathog. 12 (2016) e1005793.
Crossref Google Scholar
[66]

K.R. Chung, Stress response and pathogenicity of the necrotrophic fungal pathogen Alternaria alternata, Scientifica 2012 (2012) 635431.
Crossref Google Scholar
[67]

E.M. Govrin, A. Levine, The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea, Curr. Biol. 10 (2000) 751-757.
Crossref Google Scholar
[68]

Y.B. Li, L.B. Han, H.Y. Wang, J. Zhang, S.T. Sun, D.Q. Feng, C.L. Yang, Y.D. Sun, N.Q. Zhong, G.X. Xia, The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton, Plant Physiol. 170 (2016) 2392-2406.
Crossref Google Scholar
[69]

L.U. Long, J.R. Zhao, F.C. Xu, W.W. Yang, P. Liao, Y.A. Gao, W. Gao, C.P. Song, Silencing of GbANS reduces cotton resistance to Verticillium dahliae through decreased ROS scavenging during the pathogen invasion process, Plant Cell Tissue Organ Cult. 135 (2018) 213-221.
Crossref Google Scholar
[70]

A.F. Miller, Superoxide dismutases: ancient enzymes and new insights, FEBS Lett. 586 (2012) 585-595.
Crossref Google Scholar
The Crop Journal
Volume 10 Issue 4,
August 2022
Pages 1026-1036
DOI: 10.1016/j.cj.2021.12.010
Cite this article:
Miao Y, Chen K, Deng J, et al. miR398b negatively regulates cotton immune responses to Verticillium dahliae via multiple targets. The Crop Journal, 2022, 10(4): 1026-1036. https://doi.org/10.1016/j.cj.2021.12.010

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Received: 02 September 2021
Revised: 11 November 2021
Accepted: 26 December 2021
Published: 24 January 2022
© 2022 Crop Science Society of China and Institute of Crop Science, CAAS.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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