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Promoters of Arabidopsis Casein kinase I-like 2 and 7 confer specific high-temperature response in anther

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(1) We systematically analyze the promoter activities of AtCKLs in various tissues; (2) AtCKL2 and AtCKL7 were expressed in early developmental anthers under high temperature (HT) conditions; (3) AtMYB24 may function as a positive regulator of AtCKL2 and AtCKL7 expression under HT.

Abstract

High temperature (HT) can seriously impede plant growth and development, causing severe loss of crop production. In Arabidopsis, AtCKL genes show high similarity to GhCKI, a gene reported to disrupt tapetal programmed cell death in cotton. However, most of AtCKL genes are not well characterized. Here, we systematically analyzed the expression patterns of AtCKLs in various tissues. The expression of AtCKL2 and AtCKL7 was induced in early anther development under HT, which is similar to the case of GhCKI. In silico analysis of AtCKL2 and AtCKL7 promoters indicated that four types of transcription factors (TFs) (MADS, NAC, WRKY and R2R3-MYB) might bind to AtCKL2 and AtCKL7 promoters. Furthermore, three MADS, three NAC, one WRKY, and three R2R3-MYB TFs were up-regulated in stage 1–8 anthers and three R2R3-MYB TFs were up-regulated in stage 9–10 anthers under HT, implying the important roles of R2R3-MYB genes in the response of anthers to HT. Among the R2R3-MYB genes, AtMYB24 showed the similar expression as AtCKL2 and AtCKL7 in the anthers under HT. Additionally, yeast one-hybrid and dual-luciferase reporter system assays verified that AtMYB24 could bind to AtCKL2 and AtCKL7 promoters and activate the expression of these two genes. In brief, this study provides the overall expression profiles of AtCKLs, useful information for unraveling the molecular mechanism of AtCKL2 and AtCKL7 gene expression in early anther development under HT, and important clues for elucidating the mechanism of transcriptional regulation of CKI genes in plant anther under HT, which are critical to the reduction of crop yield loss resulting from HT.

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References

  • Abiko M, Akibayashi K, Sakata T, Kimura M, Kihara M, Itoh K, Asamizu E, Sato S, Takahashi H, Higashitani A (2005) High-temperature induction of male sterility during barley (Hordeum vulgare L.) anther development is mediated by transcriptional inhibition. Sex Plant Reprod 18:91–100

    Article  CAS  Google Scholar 

  • Chen C, Letnik I, Hacham Y, Dobrev P, Ben-Daniel BH, Vanková R, Amir R, Miller G (2014) ASCORBATE PEROXIDASE6 protects Arabidopsis desiccating and germinating seeds from stress and mediates cross talk between reactive oxygen species, abscisic acid, and auxin. Plant Physiol 166:370–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Ye JZ, Guo XH, Chang HP, Yuan CY, Wang Y, Hu S, Liu XM, Li XS (2012) Arabidopsis casein kinase 1-like 2 involved in abscisic acid signal transduction pathways. J Plant Interact 9:19–25

    Article  CAS  Google Scholar 

  • Deng FL, Tu LL, Tan JF, Li Y, Nie YC, Zhang XL (2012) GbPDF1 is involved in cotton fiber initiation via the core cis-element HDZIP2ATATHB2. Plant Physiol 158:890–904

    Article  CAS  PubMed  Google Scholar 

  • Dharmawardhana DP, Ellis BE, Carlson JE (1992) Characterization of vascular lignification in Arabidopsis thaliana. Can J Bot 70:2238–2244

    Article  CAS  Google Scholar 

  • Dornelas MC, Patreze CM, Angenent GC, Immink RGH (2011) MADS: the missing link between identity and growth? Trends Plant sci 16:89–97

    Article  CAS  PubMed  Google Scholar 

  • Duarte P, Ribeiro D, Carqueijeiro I, Bettencourt S, Sottomayor M (2016) Protoplast transformation as a plant-transferable transient expression system. In: Fett-Neto A (ed) Biotechnology of plant secondary metabolism. Methods in molecular biology, vol 1405. Humana Press, New York, pp 137–148

    Chapter  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant sci 15:573–581

    Article  CAS  PubMed  Google Scholar 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217–218:109–119

    Article  CAS  PubMed  Google Scholar 

  • Higginson T, Li SF, Parish RW (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. Plant J 35:177–192

    Article  CAS  PubMed  Google Scholar 

  • Honys D, Oh SA, Reňák D, Donders M, Šolcová B, Johnson JA, Boudová R, Twell D (2006) Identification of microspore-active promoters that allow targeted manipulation of gene expression at early stages of microgametogenesis in Arabidopsis. BMC Plant Biol 6:31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann JL, Meyerowitz EM (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360

    Article  CAS  PubMed  Google Scholar 

  • Jiao YN, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang HY, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100

    Article  CAS  PubMed  Google Scholar 

  • Joseph MP, Papdi C, Kozma-Bognár L, Nagy I, López-Carbonell M, Rigo G, Koncz C, Szabados L (2014) The Arabidopsis ZINC FINGER PROTEIN3 interferes with abscisic acid and light signaling in seed germination and plant development. Plant Physiol 165:1203–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SY, Hong CB, Lee I (2001) Heat shock stress causes stage-specific male sterility in Arabidopsis thaliana. J Plant Res 114:301–307

    Article  Google Scholar 

  • Kim D, Cho YH, Ryu H, Kim Y, Kim TH, Hwang I (2013) BLH1 and KNAT3 modulate ABA responses during germination and early seedling development in Arabidopsis. Plant J 75:755–766

    Article  CAS  PubMed  Google Scholar 

  • Knippschild U, Gocht A, Wolff S, Huber N, Löhler J, Stöter M (2005) The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell Signal 17:675–689

    Article  CAS  PubMed  Google Scholar 

  • Lee JY, Taoka K, Yoo BC, Ben-Nissan G, Kim DJ, Lucas WJ (2005) Plasmodesmal-associated protein kinase in tobacco and Arabidopsis recognizes a subset of non-cell-autonomous proteins. Plant cell 17:2817–2831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li SF, Higginson T, Parish RW (1999) A novel MYB-related gene from Arabidopsis thaliana expressed in developing anthers. Plant Cell Physiol 40:343–347

    Article  CAS  PubMed  Google Scholar 

  • Li XW, Gao XQ, Wei Y, Deng L, Ouyang YD, Chen GX, Li XH, Zhang QF, Wu CY (2011) Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-box Adenosine 5′-triphosphate-dependent RNA helicases regulates tapetum degeneration. Plant cell 23:1416–1434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Jiang J, Du ML, Li L, Wang XL, Li XB (2013) A cotton gene encoding MYB-like transcription factor is specifically expressed in pollen and is involved in regulation of late anther/pollen development. Plant Cell Physiol 54:893–906

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Xu ZH, Luo D, Xue HW (2003) Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. Plant J 36:189–202

    Article  CAS  PubMed  Google Scholar 

  • Mathelier A, Fornes O, Arenillas DJ, Chen CY, Denay G, Lee J, Shi W, Shyr C, Tan G, Worsley-Hunt R, Zhang AW, Parcy F, Lenhard B, Sandelin A, Wasserman WW (2016) JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles. Nucleic Acids Res 44:D110–D115

    Article  CAS  PubMed  Google Scholar 

  • Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Min L, Zhu LF, Tu LL, Deng FL, Yuan DJ, Zhang XL (2013) Cotton GhCKI disrupts normal male reproduction by delaying tapetum programmed cell death via inactivating starch synthase. Plant J 75:823–835

    Article  CAS  PubMed  Google Scholar 

  • Min L, Li YY, Hu Q, Zhu LF, Gao WH, Wu YL, Ding YH, Liu SM, Yang XY, Zhang XL (2014) Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton. Plant Physiol 164:1293–1308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Min L, Hu Q, Li YY, Xu J, Ma YZ, Zhu LF, Yang XY, Zhang XL (2015) LEAFY COTYLEDON1-CASEIN KINASE I-TCP15-PHYTOCHROME INTERACTING FACTOR4 network regulates somatic embryogenesis by regulating auxin homeostasis. Plant Physiol 169:2805–2821

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant cell 17:2993–3006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67:483–493

    Article  CAS  PubMed  Google Scholar 

  • Oshino T, Abiko M, Saito R, Ichiishi E, Endo M, Kawagishi-Kobayashi M, Higashitani A (2007) Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants. Mol Genet Genomics 278:31–42

    Article  CAS  PubMed  Google Scholar 

  • Ou B, Yin KQ, Liu SN, Yang Y, Gu T, Wing Hui JM, Zhang L, Miao J, Kondou Y, Matsui M, Gu HY, Qu LJ (2011) A high-throughput screening system for Arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation. Mol Plant 4:546–555

    Article  CAS  PubMed  Google Scholar 

  • Pattanaik S, Patra B, Singh SK, Yuan L (2014) An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Front Plant Sci 5:259

    Article  PubMed  PubMed Central  Google Scholar 

  • Peet MM, Sato S, Gardner RG (1998) Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant Cell Environ 21:225–231

    Article  Google Scholar 

  • Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995

    Article  CAS  PubMed  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant sci 17:369–381

    Article  CAS  PubMed  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:11664–11669

    Article  CAS  PubMed  Google Scholar 

  • Serna L, Martin C (2006) Trichomes: different regulatory networks lead to convergent structures. Trends Plant sci 11:274–280

    Article  CAS  PubMed  Google Scholar 

  • Sorensen AM, Kröber S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423

    Article  CAS  PubMed  Google Scholar 

  • Steiner-Lange S, Unte US, Eckstein L, Yang CY, Wilson ZA, Schmelzer E, Dekker K, Saedler H (2003) Disruption of Arabidopsis thaliana MYB26 results in male sterility due to non-dehiscent anthers. Plant J 34:519–528

    Article  CAS  PubMed  Google Scholar 

  • 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 Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan ST, Dai C, Liu HT, Xue HW (2013) Arabidopsis casein kinase 1 proteins CK1.3 and CK1.4 phosphorylate cryptochrome 2 to regulate blue light signaling. Plant cell 25:2618–2632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson D, Regev A, Roy S (2015) Comparative analysis of gene regulatory networks: from network reconstruction to evolution. Annu Rev Cell Dev Biol 31:399–428

    Article  CAS  PubMed  Google Scholar 

  • Tuazon PT, Traugh JA (1991) Casein kinase I and II—multipotential serine protein kinases: structure, function, and regulation. Adv Second Messenger Phosphoprotein Res 23:123–164

    CAS  PubMed  Google Scholar 

  • Verelst W, Saedler H, Münster T (2007a) MIKC* MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters. Plant Physiol 143:447–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verelst W, Twell D, de Folter S, Immink R, Saedler H, Münster T (2007b) MADS-complexes regulate transcriptome dynamics during pollen maturation. Genome Biol 8(11):R249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–1350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang LQ, Guo K, Li Y, Tu YY, Hu HZ, Wang BR, Cui XC, Peng LC (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10(1):282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang MK, Yu DS, Guo XH, Cui Y, Li XS, Zhang JH, Zhao LJ, Chang HP, Hu S, Zhang C, Shi JC, Liu XM (2011) Casein kinase 1-like 3 is required for abscisic acid regulation of seed germination, root growth, and gene expression in arabidopsis. Afr J Biotechnol 10:13219–13229

    CAS  Google Scholar 

  • Wang MJ, Yuan DJ, Gao WH, Li Y, Tan JF, Zhang XL (2013) A comparative genome analysis of PME and PMEI families reveals the evolution of pectin metabolism in plant cell walls. PLoS ONE 8(8):e72082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellmer F, Riechmann JL, Alves-Ferreira M, Meyerowitz EM (2004) Genome-wide analysis of spatial gene expression in Arabidopsis flowers. Plant cell 16:1314–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39

    Article  CAS  PubMed  Google Scholar 

  • Wu YL, Min L, Wu ZC, Yang L, Zhu LF, Yang XY, Yuan DJ, Guo XP, Zhang XL (2015) Defective pollen wall contributes to male sterility in the male sterile line 1355A of cotton. Sci Rep 5

  • Yang XY, Li JG, Pei M, Gu H, Chen ZL, Qu LJ (2007) Over-expression of a flower-specific transcription factor gene AtMYB24 causes aberrant anther development. Plant Cell Rep 26:219–228

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A (2003a) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130:4859–4869

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Gonzalez A, Zhao MZ, Payne CT, Lloyd A (2003b) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130:4859–4869

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Sun YJ, Timofejeva L, Chen CB, Grossniklaus U, Ma H (2006a) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Henriques R, Lin SS, Niu QW, Chua NH (2006b) Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat protoc 1:641–646

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liang WQ, Yang XJ, Luo X, Jiang N, Ma H, Zhang DB (2010) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22:672–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XW, Li JP, Liu A, Zou J, Zhou XY, Xiang JH, Rerksiri W, Peng Y, Xiong XY, Chen XB (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS ONE 7(11):e49652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao MZ, Morohashi K, Hatlestad G, Grotewold E, Lloyd A (2008) The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135:1991–1999

    Article  CAS  PubMed  Google Scholar 

  • Zhao HY, Zhang HM, Cui P, Ding F, Wang GC, Li RJ, Jenks MA, Lü SY, Xiong LM (2014) The putative E3 ubiquitin ligase ECERIFERUM9 regulates abscisic acid biosynthesis and response during seed germination and postgermination growth in Arabidopsis. Plant Physiol 165:1255–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao SJ, Wu YX, He YQ, Wang YR, Xiao J, Li L, Wang YP, Chen X, Xiong W, Wu Y (2015) RopGEF2 is involved in ABA-suppression of seed germination and post-germination growth of Arabidopsis. Plant J 84:886–899

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277

    Article  CAS  PubMed  Google Scholar 

  • Zou CS, Jiang WB, Yu DQ (2010) Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot 61:3901–3914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Daiyin Chao (National Key Laboratory of Plant Molecular Genetics, Chinese Academy of Sciences Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, China) for kindly providing myb24 (SALK_017221C) mutant seeds. This work was supported by the Fundamental Research Funds for the Central Universities (Program No. 2662016QD013), the National Natural Science Foundation of China (31401423) and the National Key Research and Development Program of China (2018YFD0100403).

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YL carried out the experiment with LZ, QH, YW, JL, SX, and YM, and wrote the main manuscript text. LZ, LM and XZ designed and supervised the research and revised the manuscript. All authors reviewed the manuscript.

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Correspondence to Ling Min or Longfu Zhu.

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Li, Y., Min, L., Zhang, L. et al. Promoters of Arabidopsis Casein kinase I-like 2 and 7 confer specific high-temperature response in anther. Plant Mol Biol 98, 33–49 (2018). https://doi.org/10.1007/s11103-018-0760-7

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