The role of the MAP kinase−kinase protein StMKK1 in potato immunity to different pathogens

Xiaokang Chen , Wenbin Wang , Pingping Cai , Ziwei Wang , Tingting Li , Yu Du

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 117

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :117 DOI: 10.1038/s41438-021-00556-5
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The role of the MAP kinase−kinase protein StMKK1 in potato immunity to different pathogens
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Abstract

Mitogen-activated protein kinase (MAPK) cascades play important roles in plant immunity. Previously, we reported that the potato StMKK1 protein negatively regulates Nicotiana benthamiana resistance to Phytophthora infestans. However, the functions of StMKK1 in potato immunity are unknown. To investigate the roles of StMKK1 in potato resistance to different pathogens, such as the potato late-blight pathogen P. infestans, the bacterial wilt pathogen Ralstonia solanacearum, and the gray-mold fungal pathogen Botrytis cinerea, we generated StMKK1 transgenic lines and investigated the response of potato transformants to destructive oomycete, bacterial, and fungal pathogens. The results showed that overexpression and silencing of StMKK1 do not alter plant growth and development. Interestingly, we found that StMKK1 negatively regulated potato resistance to the hemibiotrophic/biotrophic pathogens P. infestans and R. solanacearum, while it positively regulated potato resistance to the necrotrophic pathogen B. cinerea. Further investigation showed that overexpression of StMKK1 suppressed potato pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and salicylic acid (SA)-related responses, while silencing of StMKK1 enhanced PTI and SA-related immune responses. Taken together, our results showed that StMKK1 plays dual roles in potato defense against different plant pathogens via negative regulation of PTI and SA-related signaling pathways.

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Xiaokang Chen, Wenbin Wang, Pingping Cai, Ziwei Wang, Tingting Li, Yu Du. The role of the MAP kinase−kinase protein StMKK1 in potato immunity to different pathogens. Horticulture Research, 2021, 8 (1) : 117 DOI:10.1038/s41438-021-00556-5

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References

[1]

Govers, F., Drenth, A. & Pieterse, C. M. J. in Plant Relationships Part B (eds Carroll, G. C. & Tudzynski, P.) 17-36 (Springer Berlin Heidelberg, 1997).

[2]

Haverkort, A. J. et al. Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Res. 51, 47-57 (2008).

[3]

Genin, S . Molecular traits controlling host range and adaptation to plants in Ralstonia solanacearum. N. Phytologist 187, 920-928 (2010).

[4]

van Kan, J. A. L. Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11, 247-253 (2006).

[5]

Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006).

[6]

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

[7]

Cui, H. T., Tsuda, K. & Parker, J. E. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66, 487-511 (2015).

[8]

Davis, R. J. Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252 (2000).

[9]

Chang, L. F. & Karin, M. Mammalian MAP kinase signaling cascades. Nature 410, 37-40 (2001).

[10]

Jonak, C., Okresz, L., Bogre, L. & Hirt, H . Complexity, cross talk and integration of plant MAP kinase signaling. Curr. Opin. Plant Biol. 5, 415-424 (2002).

[11]

Rodriguez, M. C. S., Petersen, M. & Mundy, J. Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61, 621-649 (2010).

[12]

Pitzschke, A., Schikora, A. & Hirt, H. MAPK cascade signaling networks in plant defence. Curr. Opin. Plant Biol. 12, 421-426 (2009).

[13]

Pedley, K. F. & Martin, G. B. Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol. 8, 541-547 (2005).

[14]

Asai, T. et al. MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415, 977-983 (2002).

[15]

Mao, G. H. et al. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639-1653 (2011).

[16]

Gao, M. H. et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190-1198 (2008).

[17]

Doczi, R. et al. The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19, 3266-3279 (2007).

[18]

Lu, W., Chu, X., Li, Y., Wang, C. & Guo, X. Cotton GhMKK1 induces the tolerance of salt and drought stress, and mediates defence responses to pathogen infection in transgenic Nicotiana benthamiana. PLoS One 8, e68503 (2013).

[19]

Cai, G. et al. ZmMKK1, a novel group A mitogen-activated protein kinase kinase gene in maize, conferred chilling stress tolerance and was involved in pathogen defense in transgenic tobacco. Plant Sci. 214, 57-73 (2014).

[20]

Jagodzik, P., Tajdel-Zielinska, M., Ciesla, A., Marczak, M. & Ludwikow, A. Mitogen-activated protein kinase cascades in plant hormone signaling. Front. Plant Sci. 9, 1387 (2018).

[21]

Li, X. et al. Tomato SlMKK2 and SlMKK4 contribute to disease resistance against Botrytis cinerea. BMC Plant Biol. 14, 166 (2014).

[22]

Brader, G., Djamei, A., Teige, M., Palva, E. T. & Hirt, H. The MAP kinase kinase MKK2 affects disease resistance in Arabidopsis. Mol. Plant-Microbe Interact. 20, 589-596 (2007).

[23]

Hamel, L.-P. et al. Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci. 11, 192-198 (2006).

[24]

Chen, X., Li, F., Wang, W., Shan, W. & Du, Y. Construction of RNA interference vector to silence StMKK1 in potato and development of StMKK1-silenced transgenic potato lines. Acta Agriculturae Boreal.-occidentalis Sin. 30, 1822-1830 (2020).

[25]

Bouwmeester, K. et al. The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in solanaceous plants. Plant Biotechnol. J. 12, 10-16 (2014).

[26]

Du, Y. et al. Phytophthora infestans RXLR effector PITG20303 targets a potato MKK1 protein to suppress plant immunity. N. Phytologist 229, 501-515 (2021).

[27]

Wang, Y., Bouwmeester, K., Beseh, P., Shan, W. & Govers, F. Phenotypic analyses of Arabidopsis T-DNA insertion lines and expression profiling reveal that multiple L-type lectin receptor kinases are involved in plant immunity. Mol. Plant-Microbe Interact. 27, 1390-1402 (2014).

[28]

Du, Y., Overdijk, E. J. R., Berg, J. A., Govers, F. & Bouwmeester, K. Solanaceous exocyst subunits are involved in immunity to diverse plant pathogens. J. Exp. Botany 69, 655-666 (2018).

[29]

Mengiste, T. Plant immunity to necrotrophs. Annu. Rev. Phytopathol. 50, 267-294 (2012).

[30]

Pan, Q. et al. RTP1 encodes a novel endoplasmic reticulum (ER)-localized protein in Arabidopsis and negatively regulates resistance against biotrophic pathogens. N. Phytologist 209, 1641-1654 (2016).

[31]

Cui, H. et al. Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host Microbe 7, 164-175 (2010).

[32]

Spoel, S. H., Johnson, J. S. & Dong, X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl Acad. Sci. 104, 18842-18847 (2007).

[33]

Zhang, Z. et al. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11, 253-263 (2012).

[34]

Zhang, Z. et al. The NLR protein SUMM2 senses the disruption of an immune signaling MAP kinase cascade via CRCK3. EMBO Rep. 18, 292-302 (2016).

[35]

Kong, Q. et al. The MEKK1-MKK1/MKK2-MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24, 2225-2236 (2012).

[36]

Yang, K. Y., Liu, Y. & Zhang, S. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl Acad. Sci. 98, 741-746 (2001).

[37]

Popescu, S. C. et al. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23, 80-92 (2008).

[38]

Jiang, L., Chen, Y., Luo, L. & Peck, S. C. Central roles and regulatory mechanisms of dual-specificity MAPK phosphatases in developmental and stress signaling. Front. Plant Sci. 9, 1697 (2018).

[39]

Liu, Y., Shepherd, E. G. & Nelin, L. D. MAPK phosphatases-regulating the immune response. Nat. Rev. Immunol. 7, 202-212 (2007).

[40]

Sun, K. et al. Silencing of six susceptibility genes results in potato late blight resistance. Transgenic Res. 25, 731-742 (2016).

[41]

Fan, G. et al. A Phytophthora capsici RXLR effector targets and inhibits a plant PPIase to suppress endoplasmic reticulum-mediated immunity. Mol. Plant 11, 1067-1083 (2018).

[42]

Zhang, L. & van Kan, J. A. L. Botrytis cinerea mutants deficient in D-galacturonic acid catabolism have a perturbed virulence on Nicotiana benthamiana and Arabidopsis, but not on tomato. Mol. Plant Pathol. 14, 19-29 (2012).

[43]

Wang, H. et al. A quick and efficient hydroponic potato infection method for evaluating potato resistance and Ralstonia solanacearum virulence. Plant Methods 15, 145 (2019).

[44]

Li, L. et al. Activation-dependent destruction of a co-receptor by a Pseudomonas syringae effector dampens plant immunity. Cell Host Microbe 20, 504-514 (2016).

[45]

Zhou, X. et al. StMYB44 negatively regulates phosphate transport by suppressing expression of PHOSPHATE1 in potato. J. Exp. Botany 68, 1265-1281 (2017).

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