Abstract
Key message
The application of flagellin 22 (flg22), the most widely studied PAMP, enhance crop cold tolerance. ICE1-CBF pathway and SA signaling is involved in the alleviation of cold injury by flg22 treatment.
Abstract
Pathogen infection cross-activates cold response and increase cold tolerance of host plants. However, it is not possible to use the infection to increase cold tolerance of field plants. Here flagellin 22 (flg22), the most widely studied PAMP (pathogen-associated molecular patterns), was used to mimic the pathogen infection to cross-activate cold response. Flg22 treatment alleviated the injury caused by freezing in Arabidopsis, oilseed and tobacco. In Arabidopsis, flg22 activated the expression of immunity and cold-related genes. Moreover, the flg22 induced alleviation of cold injury was lost in NahG transgenic line (SA-deficient), sid2-2 and npr1-1 mutant plants, and flg22-induced expression of cold tolerance-related genes, which indicating that salicylic acid signaling pathway is required for the alleviation of cold injury by flg22 treatment. In short flg22 application can be used to enhance cold tolerance in field via a salicylic acid-depended pathway.
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References
Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539
Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451
Conrath U, Beckers GJ, Langenbach CJ, Jaskiewicz MR (2015) Priming for enhanced defense. Annu Rev Phytopathol 53:97–119
Dempsey DA, Vlot MCW, Daniel FK (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book/am Soc Plant Biol 9:e0156
Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Dewdney J (2009) Erratum: Activation of defense response pathways by OGs and Flg22 elicitors in arabidopsis seedlings. Mol Plant 2:838
Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552
Jia Y, Ding Y, Shi Y, Zhang X, Gong Z, Yang S (2016) The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol 212:345–353
Karan R, Subudhi PK (2012) A stress inducible SUMO conjugating enzyme gene (SaSce9) from a grass halophyte Spartina alterniflora enhances salinity and drought stress tolerance in Arabidopsis. BMC Plant Biol 12:187
Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376
Kim YS, An C, Park S, Gilmour SJ, Wang L, Renna L, Brandizzi F, Grumet R, Thomashow MF (2017) CAMTA-mediated regulation of salicylic acid immunity pathway genes in Arabidopsis exposed to low temperature and pathogen infection. Plant Cell 29:2465–2477
Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337
Muthamilarasan M, Prasad M (2013) Plant innate immunity: an updated insight into defense mechanism. J Biosci 38:433–449
Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci 101:3985–3990
Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS (2013) Tell me more: roles of NPRs in plant immunity. Trends Plant Sci 18:402–411
Rhaman MS, Imran S, Rauf F, Khatun M, Baskin CC, Murata Y, Hasanuzzaman M (2020) Seed priming with phytohormones: an effective approach for the mitigation of abiotic stress. Plants (basel) 10:37
Rivas-San VM, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338
Saijo Y, Loo EP (2020) Plant immunity in signal integration between biotic and abiotic stress responses. New Phytol 225:87–104
Schenke D, Utami HP, Zhou Z, Gallegos M-T, Cai D (2019) Suppression of UV–B stress induced flavonoids by biotic stress: is there reciprocal crosstalk? Plant Physiol Biochem 134:53–63
Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671
Serrano M, Kanehara K, Torres M, Yamada K, Tintor N, Kombrink E, Schulze-Lefert P, Saijo Y (2012) Repression of sucrose/ultraviolet B light-induced flavonoid accumulation in microbe-associated molecular pattern-triggered immunity in Arabidopsis. Plant Physiol 58:408–422
Shi Y, Ding Y, Yang S (2018) Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 23:623–637
Singh P, Yekondi S, Chen PW, Tsai CH, Yu CW, Wu K, Zimmerli L (2014) Environmental history modulates Arabidopsis pattern triggered immunity in a HISTONE ACETYLTRANSFERASE1-dependent manner. Plant Cell 26:2676–2688
Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43
Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53:763–775
Tuang ZK, Wu Z, Jin Y, Wang Y, Oo PPZ, Zuo G, Shi H, Yang W (2020) Pst DC3000 infection alleviates subsequent freezing and heat injury to host plants via a salicylic acid-dependent pathway in Arabidopsis. Plant Cell Environ 43:801–817
Ul Haq S, Khan A, Ali M, Khattak AM, Gai WX, Zhang HX, Wei AM, Gong ZH (2019) Heat shock proteins: dynamic biomolecules to counter plant biotic and abiotic stresses. Int J Mol Sci 20:5321
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565
Wu Z, Han S, Zhou H, Tuang ZK, Wang Y, Jin Y, Shi H, Yang W (2019) Cold stress activates disease resistance in Arabidopsis thaliana through a salicylic acid dependent pathway. Plant Cell Environ 42:2645–2663
Wyrsch I, Domínguez-Ferreras A, Geldner N, Boller T (2015) Tissue-specific FLAGELLIN-SENSING 2 (FLS2) expression in roots restores immune responses in Arabidopsis fls2 mutants. New Phytol 206:774–784
Yi SY, Shirasu K, Moon JS, Lee SG, Kwon SY (2014) The activated SA and JA signaling pathways have an influence on flg22-triggered oxidative burst and callose deposition. PLoS ONE 9(2):e88951
Zhang Y, Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol 50:29–36
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324
Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767
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This work was financially supported by the National Natural Science Foundation of China (Grant numbers 31470365 and 31700216).
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WY conceived and designed research. ZT, YJ, YW and ZW conducted experiments. YJ wrote the manuscript. All authors read and approved the manuscript.
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Communicated by Ying-Tang Lu.
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Jin, Y., Tuang, Z.K., Wang, Y. et al. Potential roles for pattern molecule of PAMP-triggered immunity in improving crop cold tolerance. Plant Cell Rep 41, 337–345 (2022). https://doi.org/10.1007/s00299-021-02811-4
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DOI: https://doi.org/10.1007/s00299-021-02811-4