Regulation of maize growth and immunity by ZmSKI3-mediated RNA decay and post-transcriptional gene silencing

Abstract

Disease resistance is often associated with compromised plant growth and yield due to defense-growth tradeoffs. However, key components and mechanisms underlying the defense-growth tradeoffs are rarely explored in maize. In this study, we find that ZmSKI3, a putative subunit of the SUPERKILLER (SKI) complex that mediates the 3′-5′ degradation of RNA, regulates both plant development and disease resistance in maize. The Zmski3 mutants showed retarded plant growth and constitutively activated defense responses, while the ZmSKI3 overexpression lines are more susceptible to Curvularia lunata and Bipolaris maydis. Consistently, the expression of defense-related genes was generally up-regulated, while expressions of growth-related genes were mostly down-regulated in leaves of the Zmski3-1 mutant compared to that of wild type. In addition, 223 differentially expressed genes that are up-regulated in Zmski3-1 mutant but down-regulated in the ZmSKI3 overexpression line are identified as potential target genes of ZmSKI3. Moreover, small interfering RNAs targeting the transcripts of the defense- and growth-related genes are differentially accumulated, likely to combat the increase of defense-related transcripts but decrease of growth-related transcripts in Zmski3-1 mutant. Taken together, our study indicates that plant growth and immunity could be regulated by both ZmSKI3-mediated RNA decay and post-transcriptional gene silencing in maize.

Keywords

defense-growth tradeoffs / disease resistance / maize / plant growth / PTGS / RNA decay / ZmSKI3

References

[1] Barghahn, S.,Saridis, G.,Mantz, M.,Meyer, U.,Mellüh, J.C.,Misas Villamil, J.C.,Huesgen, P.F., and Doehlemann, G. (2023). Combination of transcriptomic, proteomic, and degradomicprofiling reveals common and distinct patterns of pathogen-induced cell death in maize. Plant J. 116:574–596.

[2] Ding, Y.Z.,Murphy, K.M.,Poretsky, E.,Mafu, S.,Yang, B.,Char, S.N.,Christensen, S.A.,Saldivar, E.,Wu, M.X.,Wang, Q., et al. (2019). Multiple genes recruited from hormone pathways partition maize diterpenoid defences. Nat. Plants 5:1043–1056.

[3] Ding, Y.Z.,Weckwerth, P.R.,Poretsky, E.,Murphy, K.M.,Sims, J.,Saldivar, E.,Christensen, S.A.,Char, S.N.,Yang, B.,Tong, A., et al. (2020). Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity. Nat. Plants 6:1375–1388.

[4] Dorcey, E.,Rodriguez-Villalon, A.,Salinas, P.,Santuari, L.,Pradervand, S.,Harshman, K., and Hardtke, C.S. (2012). Context-dependent dual role of SKI8 homologs in mRNA synthesis and turnover. PLoS Genet. 8: e1002652.

[5] Fabre, A.,Martinez-Vinson, C.,Goulet, O., and Badens, C. (2013). Syndromic diarrhea/Tricho-hepato-enteric syndrome. Orphanet J. Rare Dis. 8:5.

[6] Förster, C.,Handrick, V.,Ding, Y.Z.,Nakamura, Y.,Paetz, C.,Schneider, B.,Castro-Falcón, G.,Hughes, C.C.,Luck, K.,Poosapati, S., et al. (2021). Biosynthesis and antifungal activity of fungus-induced O-methylated flavonoids in maize. Plant Physiol. 188:167–190.

[7] Freh, M.,Gao, J.L.,Petersen, M., and Panstruga, R. (2022). Plant autoimmunity-fresh insights into an old phenomenon. Plant Physiol. 188:1419–1434.

[8] Fu, D.D.,Li, J.Y.,Yang, X.,Li, W.L.,Zhou, Z.R.,Xiao, S.Q., and Xue, C.S. (2022). Iron redistribution induces oxidative burst and resistance in maize against Curvularia lunata. Planta 256:46–60.

[9] Ge, C.X.,Wang, Y.G.,Lu, S.P.,Zhao, X.Y.,Hou, B.K.,Balint-Kurti, P.J., and Wang, G.F. (2021). Multi-omics analyses reveal the regulatory network and the function of ZmUGTs in maize defense response. Front. Plant Sci. 12:738261.

[10] Gou, M.Y.,Balint-Kurti, P.,Xu, M.L., and Yang, Q. (2023). Quantitative disease resistance: Multifaceted players in plant defense. J. Integr. Plant Biol. 65:594–610.

[11] Guo, Q.Q.,Li, X.,Niu, L.,Jameson, P.E., and Zhou, W.B. (2021). Transcription-associated metabolomic adjustments in maize occur during combined drought and cold stress. Plant Physiol. 186:677–695.

[12] Halbach, F.,Reichelt, P.,Rode, M., and Conti, E. (2013). The yeast ski complex: Crystal structure and RNA channeling to the exosome complex. Cell 154:814–826.

[13] He, Z.H.,Webster, S., and He, S.Y. (2022). Growth-defense trade-offs in plants. Curr. Biol. 32: R634–R639.

[14] Januszyk, K., and Lima, C.D. (2014). The eukaryotic RNA exosome. Curr. Opin. Struct. Biol. 24:132–140.

[15] Jiao, Z.Y.,Tian, Y.Y.,Cao, Y.Y.,Wang, J.,Zhan, B.H.,Zhao, Z.X.,Sun, B.,Guo, C.,Ma, W.D.,Liao, Z.F., et al. (2021). A novel pathogenicity determinant hijacks maize catalase 1 to enhance viral multiplication and infection. New Phytol. 230:1126–1141.

[16] Jones, J.D.G., and Dangl, J.L. (2006). The plant immune system. Nature 444:323–329.

[17] Kidwai, M.,Ahmad, I.Z., and Chakrabarty, D. (2020). Class III peroxidase: An indispensable enzyme for biotic/abiotic stress tolerance and a potent candidate for crop improvement. Plant Cell Rep. 39:1381–1393.

[18] Kim, S.B.,Van den Broeck, L.,Karre, S.,Choi, H.,Christensen, S.A.,Wang, G.F.,Jo, Y.,Cho, W.K., and Balint-Kurti, P. (2021). Analysis of the transcriptomic, metabolomic, and gene regulatory responses to Puccinia sorghi in maize. Mol. Plant Pathol. 22:465–479.

[19] Kögel, A.,Keidel, A.,Bonneau, F.,Schäfer, I.B., and Conti, E. (2022). The human SKI complex regulates channeling of ribosome-bound RNA to the exosome via an intrinsic gatekeeping mechanism. Mol. Cell 82:756–769.

[20] Lange, H.,Ndecky, S.Y.,Gomez-Diaz, C.,Pflieger, D.,Butel, N.,Zumsteg, J.,Kuhn, L.,Piermaria, C.,Chicher, J., and Christie, M. (2019). RST1 and RIPR connect the cytosolic RNA exosome to the Ski complex in Arabidopsis. Nat. Commun. 10:3871–3882.

[21] Li, J.K.,Chen, M.Y.,Fan, T.Y.,Mu, X.H.,Gao, J.,Wang, Y.,Jing, T.,Shi, C.L.,Niu, H.B.,Zhen, S.H., et al. (2022a). Underlying mechanism of accelerated cell death and multiple disease resistance in a maize lethal leaf spot 1 allele. J. Exp. Bot. 73:3991–4007.

[22] Li, J.K.,Fan, T.Y.,Zhang, Y.,Xing, Y.,Chen, M.Y.,Wang, Y.,Gao, J.,Zhang, N.,Tian, J.J.,Zhao, C.Y., et al. (2024). Characterization and fine mapping of a maize lesion mimic mutant (Les8) with enhanced resistance to Curvularia leaf spot and southern leaf blight. Theor. Appl. Genet. 137:7.

[23] Li, S.N.,Lin, D.X.,Zhang, Y.W.,Deng, M.,Chen, Y.X.,Lv, B.,Li, B.S.,Lei, Y.,Wang, Y.P.,Zhao, L., et al. (2022b). Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 602:455–477.

[24] Li, Y.,Zhou, Y.J.,Dai, P.H.,Ren, Y.P.,Wang, Q., and Liu, X.D. (2021). Cotton Bsr-k1 modulates lignin deposition participating in plant resistance against Verticillium dahliae and Fusarium oxysporum. Plant Growth Regul. 95:283–292.

[25] Liu, M.M.,Shi, Z.Y.,Zhang, X.H.,Wang, M.X.,Zhang, L.,Zheng, K.Z.,Liu, J.Y.,Hu, X.M.,Di, C.R.,Qian, Q., et al. (2019). Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat. Plants 5:389–400.

[26] Lyon, R.M.,Johnson, E.T., and Dowd, P.F. (2024). Undesirable protein sequence variations in maize genes that confer resistance to fungal pathogens and insect pests. Plant Gene 37:100441.

[27] Ma, Y.X.,Zhou, Z.J.,Cao, H.Z.,Zhou, F.,Si, H.L.,Zang, J.P.,Xing, J.H.,Zhang, K., and Dong, J.G. (2023). Identification and expression analysis of sugar transporter family genes reveal the role of ZmSTP2 and ZmSTP20 in maize disease resistance. J. Integr. Agr. 22:3458–3473.

[28] Mafu, S.,Ding, Y.Z.,Murphy, K.M.,Yaacoobi, O.,Addison, J.B.,Wang, Q.,Shen, Z.X.,Briggs, S.P.,Bohlmann, J.,Castro-Falcon, G., et al. (2018). Discovery, biosynthesis and stress-related accumulation of dolabradiene-derived defenses in maize. Plant Physiol. 176:2677–2690.

[29] Mu, X.H.,Dai, Z.Z.,Guo, Z.Y.,Zhang, H.,Yang, J.P.,Gan, X.K.,Li, J.K.,Liu, Z.H.,Tang, J.H., and Gou, M.Y. (2022). Systematic dissection of disease resistance to southern corn rust by bulked-segregant and transcriptome analysis. Crop J. 10:426–435.

[30] Mu, X.H.,Li, J.K.,Dai, Z.Z.,Xu, L.P.,Fan, T.Y.,Jing, T.,Chen, M.Y., and Gou, M.Y. (2021). Commonly and specifically activated defense responses in maize disease lesion mimic mutants revealed by integrated transcriptomics and metabolomics analysis. Front. Plant Sci. 12:638792.

[31] Niu, Y.N.,Zhao, X.Q.,Chao, W.,Lu, P.N.,Bai, X.D., and Mao, T.T. (2023). Genetic variation, DIMBOA accumulation, and candidate gene identification in Maize multiple insect-resistance. Int. J. Mol. Sci. 24:2138–2164.

[32] Olukolu, B.A.,Wang, G.F.,Vontimitta, V.,Venkata, B.P.,Marla, S.,Ji, J.B.,Gachomo, E.,Chu, K.,Negeri, A.,Benson, J., et al. (2014). A genome-wide association study of the maize hypersensitive defense response identifies genes that cluster in related pathways. PLoS Genet. 10: e1004562.

[33] Perea-Resa, C.,Hernández-Verdeja, T.,López-Cobollo, R.,Castellano, M.M., and Salinas, J. (2012). LSM proteins provide accurate splicing and decay of selected transcripts to ensure normal Arabidopsis development. Plant Cell 24:4930–4947.

[34] Ran, X.J.,Zhao, F.,Wang, Y.J.,Liu, J.,Zhuang, Y.L.,Ye, L.H.,Qi, M.F.,Cheng, J.F., and Zhang, Y.J. (2020). Plant regulomics: A data-driven interface for retrieving upstream regulators from plant multi-omics data. Plant J. 101:237–248.

[35] Schmidt, C.,Kowalinski, E.,Shanmuganathan, V.,Defenouillere, Q.,Braunger, K.,Heuer, A.,Pech, M.,Namane, A.,Berninghausen, O.,Fromont-Racine, M., et al. (2016). The cryo-EM structure of a ribosome-Ski2-Ski3-Ski8 helicase complex. Science 354:1431–1433.

[36] Sha, G.,Sun, P.,Kong, X.J.,Han, X.Y.,Sun, Q.P.,Fouillen, L.,Zhao, J.,Li, Y.,Yang, L.,Wang, Y., et al. (2023). Genome editing of a rice CDP-DAG synthase confers multipathogen resistance. Nature 618:1017–1023.

[37] Simmons, C.,Hantke, S.,Grant, S.,Johal, G.S., and Briggs, S.P. (1998). The maize lethal leaf spot 1 mutant has elevated resistance to fungal infection at the leaf epidermis. Mol. Plant Microbe Interact. 11:1110–1118.

[38] Simmons, C.R.,Fridlender, M.,Navarro, P.A., and Yalpani, N. (2003). A maize defense-inducible gene is a major facilitator superfamily member related to bacterial multidrug resistance efflux antiporters. Plant Mol. Biol. 52:433–446.

[39] Song, W.,Wang, B.Q.,Li, X.H.,Wei, J.F.,Chen, L.,Zhang, D.M.,Zhang, W.Y., and Li, R.G. (2015). Identification of immune related LRR-containing genes in maize Zea mays (L.) by genome-wide sequence analysis. Int. J. Genomics 2015:1–11.

[40] Sun, Y.,Ma, S.J.,Liu, X.G., and Wang, G.F. (2023). The maize ZmVPS23-like protein relocates the nucleotide-binding leucine-rich repeat protein Rp1-D21 to endosomes and suppresses the defense response. Plant Cell 35:2369–2390.

[41] Wang, X.Y.,Kong, W.W.,Wang, Y.,Wang, J.H.,Zhong, L.Y.,Lao, K.W.,Dong, X.X.,Zhang, D.Y.,Huang, H.,Mo, B.X., et al. (2022). Uridylation and the SKI complex orchestrate the Calvin cycle of photosynthesis through RNA surveillance of TKL1 in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 119: e2205842119.

[42] Wu, Q.,Xu, F.,Liu, L.,Char, S.N.,Ding, Y.,Je, B.I.,Schmelz, E.,Yang, B., and Jackson, D. (2020). The maize heterotrimeric G protein β subunit controls shoot meristem development and immune responses. Proc. Natl. Acad. Sci. U. S. A. 117:1799–1805.

[43] Wulff, B.B.H., and Krattinger, S.G. (2022). The long road to engineering durable disease resistance in wheat. Curr. Opin. Biotechnol. 73:270–275.

[44] Xie, T.,Liu, Z.C., and Wang, G.G. (2020). Structural basis for monolignol oxidation by a maize laccase. Nat. Plants 6:231–237.

[45] Yang, Q.,Balint-Kurti, P., and Xu, M.L. (2017). Quantitative disease resistance: Dissection and adoption in maize. Mol. Plant 10:402–413.

[46] Yu, A.,Saudemont, B.,Bouteiller, N.,Elvira-Matelot, E.,Lepère, G.,Parent, J.-S.,Morel, J.-B.,Cao, J.,Elmayan, T., and Vaucheret, H. (2015). Second-site mutagenesis of a hypomorphic argonaute1 allele identifies SUPERKILLER3 as an endogenous suppressor of transgene posttranscriptional gene silencing. Plant Physiol. 169:1266–1274.

[47] Zhang, H.,Liu, Y.M.,Zhang, X.Y.,Ji, W.Q., and Kang, Z.S. (2023). A necessary considering factor for breeding: Growth-defense tradeoff in plants. Stress Biol. 3:6.

[48] Zhang, X.Y.,Zhu, Y.,Liu, X.D.,Hong, X.Y.,Xu, Y.,Zhu, P.,Shen, Y.,Wu, H.H.,Ji, Y.S.,Wen, X., et al. (2015). Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in Arabidopsis. Science 348:120–123.

[49] Zhang, Y.L., and Li, X. (2019). Salicylic acid: Biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50:29–36.

[50] Zhang, W.,Murphy, C., and Sieburth, L.E. (2010). Conserved RNaseII domain protein functions in cytoplasmic mRNA decay and suppresses Arabidopsis decapping mutant phenotypes. Proc. Natl. Acad. Sci. U. S. A. 107:15981–15985.

[51] Zhao, L.F., and Kunst, L. (2016). SUPERKILLER complex components are required for the RNA exosome-mediated control of cuticular wax biosynthesis in Arabidopsis inflorescence stems. Plant Physiol. 171:960–973.

[52] Zhao, Y.Z.,Lu, X.M.,Liu, C.X.,Guan, H.Y.,Zhang, M.,Li, Z.F.,Cai, H.W., and Lai, J.S. (2012). Identification and fine mapping of rhm1 locus for resistance to southern corn leaf blight in maize. J. Integr. Plant Biol. 54:321–329.

[53] Zhou, Q.Q.,Fu, Z.Y.,Li, M.Y.,Shen, Q.W.,Sun, C.R.,Feng, Y.J.,Liu, Y.,Jiang, J.J.,Qin, T.,Mao, T.L., et al. (2023). Maize tubulin folding cofactor B is required for cell division and cell growth through modulating microtubule homeostasis. New Phytol. 239:1707–1722.

[54] Zhou, S.Q.,Richter, A., and Jander, G. (2018a). Beyond defense: Multiple functions of benzoxazinoids in maize metabolism. Plant Cell Physiol. 59:1528–1537.

[55] Zhou, X.G.,Liao, H.C.,Chern, M.,Yin, J.J.,Chen, Y.F.,Wang, J.P.,Zhu, X.B.,Chen, Z.X.,Yuan, C.,Zhao, W., et al. (2018b). Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. U. S. A. 115:3174–3179.

[56] Zhu, M.,Tong, L.X.,Xu, M.L., and Zhong, T. (2021). Genetic dissection of maize disease resistance and its applications in molecular breeding. Mol. Breed. 41:32.

[57] Zinder, J.C., and Lima, C.D. (2017). Targeting RNA for processing or destruction by the eukaryotic RNA exosome and its cofactors. Gene Dev. 31:88–100.

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