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Expression and functional analysis of genes encoding cytokinin receptor-like histidine kinase in maize (Zea mays L.)

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Abstract

Cytokinin signaling is vital for plant growth and development which function via the two-component system (TCS). As one of the key component of TCS, transmembrane histidine kinases (HK) are encoded by a small gene family in plants. In this study, we focused on expression and functional analysis of cytokinin receptor-like HK genes (ZmHK) in maize. Firstly, bioinformatics analysis revealed that seven cloned ZmHK genes have different expression patterns during maize development. Secondly, ectopic expression by CaMV35S promoter in Arabidopsis further revealed that functional differentiation exists among these seven members. Among them, the ZmHK1a2-OX transgenic line has the lowest germination rate in the dark, ZmHK1-OX and ZmHK2a2-OX can delay leaf senescence, and seed size of ZmHK1-OX, ZmHK1a2-OX, ZmHK2-OX, ZmHK3b-OX and ZmHK2a2-OX was obviously reduced as compared to wild type. Additionally, ZmHK genes play opposite roles in shoot and root development; all ZmHK-OX transgenic lines display obvious shorter root length and reduced number of lateral roots, but enhanced shoot development compared with the wild type. Most notably, Arabidopsis response regulator ARR5 gene was up-regulated in ZmHK1-OX, ZmHK1a2-OX, ZmHK2-OX, ZmHK3b-OX and ZmHK2a2-OX as compared to wild type. Although the causal link between ZmHK genes and cytokinin signaling pathway is still an area to be further elucidated, these findings reflected that the diversification of ZmHK genes expression patterns and functions occurred in the course of maize evolution, indicating that some ZmHK genes might play different roles during maize development.

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References

  • Anantharaman V, Aravind L (2001) The CHASE domain: a predicted ligand binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem Sci 26:579–582

    Article  CAS  PubMed  Google Scholar 

  • Brenner W, Romanov G, Bürkle L, Schmülling T (2005) Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J 44:314–333

    Article  CAS  PubMed  Google Scholar 

  • Bruggmann R, Bharti AK, Gundlach H, Lai J, Young S, Pontaroli AC et al (2006) Uneven chromosome contraction and expansion in the maize genome. Genome Res 16:1241–1251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chu ZX, Ma Q, Lin YX, Tang XL, Zhou YQ, Zhu SW, Fan J, Cheng BJ (2011) Genome-wide identification, classification, and analysis of two-component signal system genes in maize. Genet Mol Res 10:3316–3330

    Article  CAS  PubMed  Google Scholar 

  • D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011) Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J 65:972–979

    Article  PubMed  Google Scholar 

  • Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR (2008) A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol 146(1):250–264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination and longevity in Arabidopsis. Plant Physiol 122:403–413

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, Leebens-Mack J, Altman N (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23(2):469–478

    Article  CAS  PubMed  Google Scholar 

  • Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525

    Article  CAS  PubMed  Google Scholar 

  • Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J, Olszewski N, Ori N, Eshed Y, Weiss D (2005) Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17:92–102

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He P, Osaki M, Takebe M, Shinano T, Wasaki J (2005) Endogenous hormones and expression of senescence-related genes in different senescent types of maize. J Exp Bot 56:1117–1128

    Article  CAS  PubMed  Google Scholar 

  • Heyl A, Schmulling T (2003) Cytokinin signal perception and transduction. Curr Opin Plant Biol 6:480–488

    Article  CAS  PubMed  Google Scholar 

  • Hothorn M, Dabi T, Chory J (2011) Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat Chem Biol 7:766–768

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–387

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Kurata N (2006) Identification and characterization of cytokinin-signalling gene families in rice. Gene 382:57–65

    Article  CAS  PubMed  Google Scholar 

  • Jiao BB, Wang JJ, Zhu XD, Zeng LJ, Li Q, He ZH (2012) A novel protein RLS1 with NB-ARM domains is involved in chloroplast degradation during leaf senescence in rice. Mol Plant 5:205–217

    Article  CAS  PubMed  Google Scholar 

  • Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54:605–627

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA 103:814–819

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 8:115–136

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lomin SN, Yonekura-Sakakibara K, Romanov GA, Sakakibara H (2011) Ligand-binding properties and subcellular localization of maize cytokinin receptors. J Exp Bot 62:5149–5159

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lomin SN, Krivosheev DM, Steklov MY, Osolodkin DI, Romanov GA (2012) Receptor properties and features of cytokinin signaling. Acta Nat 4:31–45

    CAS  Google Scholar 

  • Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290(5494):1151–1155

    Article  CAS  PubMed  Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    Article  CAS  PubMed  Google Scholar 

  • Muñiz LM, Royo J, Gómez E, Baudot G, Paul W, Hueros G (2010) Atypical response regulators expressed in the maize endosperm transfer cells link canonical two component systems and seed biology. BMC Plant Biol 10:84

    Article  PubMed Central  PubMed  Google Scholar 

  • Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguch C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell Online 16:1365–1377

    Article  CAS  Google Scholar 

  • Otto SP, Yong P (2002) The evolution of gene duplicates. Adv Genet 46:451–483

    Article  CAS  PubMed  Google Scholar 

  • Page T, Griffiths G, Buchanan-Wollaston V (2001) Molecular and biochemical characterization of postharvest senescence in broccoli. Plant Physiol 125:718–727

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paterson AH, Bowers JE, Chapman BA (2004) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Quirino BF, Noh YS, Himelblau E, Amasino RM (2000) Molecular aspects of leaf senescence. Trends Plant Sci 5:278–282

    Article  CAS  PubMed  Google Scholar 

  • Ren B, Liang Y, Deng Y, Chen QG, Zhang J, Yang XH, Zuo JR (2009) Genome-wide comparative analysis of type-A Arabidopsis response regulator genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res 19:1178–1190

    Article  CAS  PubMed  Google Scholar 

  • Riefler M, Novak O, Strnad M, Schmulling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66:553–563

    Article  CAS  PubMed  Google Scholar 

  • Swigonova Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) On the tetraploid origin of the maize genome. Comp Funct Genomics 5:281–284

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vyroubalová S, Václavíková K, Turecková V, Novák O, Smehilová M, Hluska T, Ohnoutková L, Frébort I, Galuszka P (2009) Characterization of new maize genes putatively involved in cytokinin metabolism and their expression during osmotic stress in relation to cytokinin levels. Plant Physiol 151:433–447

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang D, Pei K, Fu Y, Sun ZX, Li SJ, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24

    Article  CAS  PubMed  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369–376

    Article  CAS  PubMed  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K, Miwa K, Yamashino T, Mizuno T (2001) The Arabidopsis AHK4 histidine kinase is a cytokinin binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–1023

    Article  CAS  PubMed  Google Scholar 

  • Yonekura-Sakakibara K, Kojima M, Yamaya T, Sakakibara H (2004) Molecular characterization of cytokinin-responsive histidine kinases in maize. Differential ligand preferences and response to cis-zeatin. Plant Physiol 134:1654–1661

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zheng B, Deng Y, Mu JY, Ji Z, Xiang TT, Niu QW, Chua N, Zuo JR (2006) Cytokinin affects circadian-clock oscillation in a phytochrome B- and Arabidopsis response regulator 4-dependent manner. Physiol Plant 127:277–292

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by Key Project of the National Natural Science Foundation of China (31230054), the National Basic Research Program of China (973 Program) (2012CB910900), National Science Found for Distinguished Young Scholars (30925023) and 863 Project of China (2012AA10A305).

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. State Key Laboratory for Agrobiotechnology, Key Laboratory of Crop Heterosis Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, 100193, China

    Bo Wang, Yanhong Chen, Baojian Guo, Muhammad Rezaul Kabir, Yingyin Yao, Huiru Peng, Chaojie Xie, Yirong Zhang, Qixin Sun & Zhongfu Ni

  2. National Plant Gene Research Centre (Beijing), Beijing, 100193, China

    Bo Wang, Yanhong Chen, Baojian Guo, Muhammad Rezaul Kabir, Yingyin Yao, Huiru Peng, Chaojie Xie, Yirong Zhang, Qixin Sun & Zhongfu Ni

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  1. Bo Wang
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  3. Baojian Guo
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  10. Zhongfu Ni
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Correspondence to Zhongfu Ni.

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Communicated by S. Hohmann.

B. Wang and Y. Chen contributed equally to this work.

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Wang, B., Chen, Y., Guo, B. et al. Expression and functional analysis of genes encoding cytokinin receptor-like histidine kinase in maize (Zea mays L.). Mol Genet Genomics 289, 501–512 (2014). https://doi.org/10.1007/s00438-014-0821-9

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