Abstract
Key message
CmBBX22, a transcription factor of chrysanthemum, was verified to confer drought tolerance in Arabidopsis thaliana.
Abstract
The BBX proteins are known to operate as regulators of plant growth and development, but as yet their contribution to the abiotic stress response has not been well defined. Here, the chrysanthemum BBX family member CmBBX22, an ortholog of AtBBX22, was found to be transcribed throughout the plant, although at varying intensity, and was induced by imposing moisture deficiency via exposure to polyethylene glycol. The heterologous, constitutive expression of this gene in Arabidopsis thaliana compromised germination and seedling growth, but enhanced the plants’ ability to tolerate drought stress. In transgenic plants challenged with abscisic acid, leaf senescence was delayed and the senescence-associated genes and chlorophyll catabolic genes SAG29, NYE1, NYE2 and NYC1 were down-regulated. We speculated that CmBBX22 may serves as a regulator in mediating drought stress tolerance and delaying leaf senescence.
Similar content being viewed by others
References
Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D (2009) Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol 150(1):463–481
Chang CS, Li YH, Chen LT, Chen WC, Hsieh WP, Shin J, Jane WN, Chou SJ, Choi G, Hu JM (2008) LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J 54(2):205–219
Chen H, Xiong L (2008) Role of HY5 in abscisic acid response in seeds and seedlings. Plant Signal Behav 3(11):986–988
Chen Z, Zhang H, Jablonowski D, Zhou X, Ren X, Hong X, Schaffrath R, Zhu JK, Gong Z (2006) Mutations in ABO1/ELO2, a subunit of holo-elongator, increase abscisic acid sensitivity and drought tolerance in Arabidopsis thaliana. Mol Cell Biol 26(18):6902
Chen S, Cui X, Chen Y, Gu C, Miao H, Gao H, Chen F, Liu Z, Guan Z, Fang W (2011) CgDREBa transgenic chrysanthemum confers drought and salinity tolerance. Environ Exp Bot 74(12):255–260
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J Cell Mol Biol 16(6):735–743
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12(4):599
Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19(7):460
Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (2016) ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant 9(9):1272
Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol CB 21(9):R346–R355
Khanna R, Kronmiller B, Maszle DR, Coupland G, Holm M, Mizuno T, Wu SH (2009) The Arabidopsis B-Box zinc finger family. Plant Cell 21(11):3416–3420
Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19(4):1362–1375
Lee IC, Hong SW, Whang SS, Lim PO, Hong GN, Koo JC (2011) Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant Cell Physiol 52(4):651–662
Lers A (2007) Environmental regulation of leaf senescence. Blackwell 26(6):108–144
Li H, Jiang H, Bu Q, Zhao Q, Sun J, Xie Q, Li C (2011) The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response. Plant Physiol 156(2):550–563
Li Z, Zhao Y, Liu X, Peng J, Guo H, Luo J (2014) LSD 2.0: an update of the leaf senescence database. Nucl Acid Res 42(Database issue):1200–1205
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408
Michal SS, Amnon L, Alon S, Guy CL, Ron P (2010) Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plant longevity. J Exp Bot 61(1):261–273
Mittal A, Gampala SS, Ritchie GL, Payton P, Burke JJ, Rock CD (2014) Related to ABA-insensitive3(ABI3)/viviparous1 and AtABI5 transcription factor coexpression in cotton enhances drought stress adaptation. Plant Biotechnol J 12(5):578–589
Munnébosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31(3):8808–8818
Nagaoka S, Takano T (2003) Salt tolerance-related protein STO binds to a Myb transcription factor homologue and confers salt tolerance in Arabidopsis. J Exp Bot 54(391):2231–2237
Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 Locus and of endogenous abscisic acid. Plant Cell 6(11):1567
Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5(7):278
Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu JK, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63(3):417–429
Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104(49):19631–19636
Rubina J, Sullivan KL, Ross C, Erridge ZA, David C, Mclachlan ARG, Brummell DA, Dijkwel PP, Hunter DA (2015) Staying green postharvest: how three mutations in the Arabidopsis chlorophyll b reductase gene NYC1 delay degreening by distinct mechanisms. J Exp Bot 66(21):6849–6862
Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2010) Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and light-harvesting complex II degradation during senescence in rice. Plant J 57(1):120–131
Scarpeci TE, Frea VS, Zanor MI, Valle EM (2017) Overexpression of AtERF019 delays plant growth and senescence and improves drought tolerance in Arabidopsis. J Exp Bot 68(3):673
Seo PJ, Park JM, Kang SK, Kim SG, Park CM (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233(1):189–200
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evolut 28(10):2731
Wang Q, Tu X, Zhang J, Chen X, Rao L (2013) Heat stress-induced BBX18 negatively regulates the thermotolerance in Arabidopsis. Mol Biol Rep 40(3):2679–2688
Wu S, Li Z, Yang L, Xie Z, Chen J, Zhang W, Liu T, Gao S, Gao J, Zhu Y (2016) NON-YELLOWING2 (NYE2), a close paralog of NYE1, plays a positive role in chlorophyll degradation in Arabidopsis. Mol Plant 9(4):624
Xu D, Li J, Gangappa SN, Hettiarachchi C, Lin F, Andersson MX, Jiang Y, Deng XW, Holm M (2014) Convergence of light and ABA signaling on the ABI5 promoter. PLos Genet 10(2):e1004197
Yang Y, Ma C, Xu Y, Wei Q, Imtiaz M, Lan H, Gao S, Cheng L, Wang M, Fei Z (2014) A zinc finger protein regulates flowering time and abiotic stress tolerance in chrysanthemum by modulating gibberellin biosynthesis. Plant Cell 26(5):2038
Yu Y, Wang J, Shi H, Gu J, Dong J, Deng XW, Huang R (2016) Salt stress and ethylene antagonistically regulate nucleocytoplasmic partitioning of COP1 to control seed germination. Plant Physiol 170(4):2340–2350
Zelicourt AD, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21(8):677–685
Zhang T, Qu Y, Wang H, Wang J, Song A, Hu Y, Chen S, Jiang J, Chen F (2017) The heterologous expression of a chrysanthemum TCP-P transcription factor CmTCP14 suppresses organ size and delays senescence in Arabidopsis thaliana. Plant Physiol Biochem 115:239–248
Zhao Y, Chan Z, Gao J, Xing L, Cao M, Yu C, Hu Y, You J, Shi H, Zhu Y (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci USA 113(7):1949
Zhou T, Yang X, Wang L, Xu J, Zhang X (2014) GhTZF1 regulates drought stress responses and delays leaf senescence by inhibiting reactive oxygen species accumulation in transgenic Arabidopsis. Plant Mol Biol 85(1–2):163–177
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31572159), the National Science Fund for Distinguished Young Scholars (31425022).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interests.
Additional information
Communicated by Günther Hahne.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, Y., Chen, H., Ping, Q. et al. The heterologous expression of CmBBX22 delays leaf senescence and improves drought tolerance in Arabidopsis. Plant Cell Rep 38, 15–24 (2019). https://doi.org/10.1007/s00299-018-2345-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-018-2345-y