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A Proteomic Approach to Analyze Differential Regulation of Proteins During Bud Outgrowth Under Apical Dominance Based on the Auxin Transport Canalization Model in Rice (Oryza sativa L.)

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Abstract

Apical dominance refers to the inhibition of shoot branching by the dominant shoot apex. The underlying mechanisms of apical dominance, especially in rice (Oryza sativa), remain a subject of debate. Here, we studied apical dominance in the indica rice variety ‘Yangdao 6’ and carried out a comparative proteomic analysis to analyze the different levels of expression of proteins after decapitation. A total of 38 differentially expressed proteins in nodes and buds were successfully identified by MALDI-TOF/TOF and these proteins comprised ten functional categories. Among them, several proteins in this study involved in signal transduction, transporters, and cytokinin biosynthesis may play an important role in the mechanism of apical dominance. In addition, qRT-PCR was used to quantitate the expression levels of several genes in rice nodes and buds. The results showed that after decapitation, the expression level of a CK synthesis gene, OsLOG7, was reduced in buds, however, expression levels of several CK synthesis genes, OsIPTs, were markedly increased in nodes, indicating that after panicle removal, cytokinins were synthesized in nodes and subsequently delivered to buds, which will trigger release from dormancy in buds. Expression levels of several strigolactone-related genes were reduced in nodes after decapitation, which may become a factor facilitating auxin transport out of buds to stems.

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References

  • Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50(8):1416–1424

    Article  CAS  PubMed  Google Scholar 

  • Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104(34):13839–13844

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Balla J, Kalousek P, Reinohl V, Friml J, Prochazka S (2011) Competitive canalization of PIN-dependent auxin flow from axillary buds controls pea bud outgrowth. Plant 65(4):571–577

    Article  CAS  Google Scholar 

  • Bangerth F (1994) Response of cytokinin concentration in the xylem exudates of bean (Phaseolus vulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance. Planta 194:439–442

    Article  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Frim J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150(1):482–493

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Muller D, Domagalsk MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137:2905–2913

    Article  CAS  PubMed  Google Scholar 

  • Ding CQ, You J, Liu ZH, Rehmani MIA, Wang SH, Li GH, Wang QS, Ding YF, Wang QS, Ding YF (2011) Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice. Plant Mol Biol Rep 29:618–625

    Article  CAS  Google Scholar 

  • Dobrev PI, Kaminek M (2002) Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J Chromatogr A 950:21–29

    Article  PubMed  Google Scholar 

  • Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12(4):211–221

    Article  CAS  PubMed  Google Scholar 

  • Dun EA, Ferguson BJ, Beveridge CA (2006) Apical dominance and shoot branching. Divergent opinions or divergent mechanisms? Plant Physiol 142(3):812–819

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158(1):487–498

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Farmer LM, Book AJ, Lee KH, Lin YL, Fu H, Vierstra RD (2010) The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis. Plant Cell 22(1):124–142

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ferguson BJ, Beveridge CA (2009) Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol 149(4):1929–1944

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayward A, Stirnberg P, Beveridge CA, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911

    Article  CAS  PubMed  Google Scholar 

  • Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S, Yoshida S, Ashikari M, Kitano H, Matsuoka M (2003) A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15:2900–2910

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huang J, Zhao X, Yu H, Ouyang Y, Wang L, Zhang Q (2009) The ankyrin repeat gene family in rice: genome-wide identification, classification and expression profiling. Plant Mol Biol 71(3):207–226

    Article  CAS  PubMed  Google Scholar 

  • Kania U, Fendrych M, Friml J (2014) Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol 4:140017

    Article  PubMed Central  PubMed  Google Scholar 

  • Li C, Bangerth F (1999) Autoinihibition of indoleacetic acid transport in the shoot of two-branched pea (Pisum sativum) plants and its relationship to correlative dominance. Physiol Plant 106:415–420

    Article  CAS  Google Scholar 

  • Liang J, Zhao L, Challis R, Leyser O (2010) Strigolactone regulation of shoot branching in chrysanthemum (Dendranthema grandiflorum). J Exp Bot 61(11):3069–3078

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21(5):1512–1525

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Y, Xu JX, Ding YF, Wang QS, Li GH, Wang SH (2011) Auxin inhibits the outgrowth of tiller buds in rice (Oryza sativa L.) by downregulating OsIPT expression and cytokinin biosynthesis in nodes. Aust J Crop Sci 5(2):169–174

    CAS  Google Scholar 

  • McMahon HT, Boucrot E (2011) Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12:517–533

    Article  CAS  PubMed  Google Scholar 

  • Molendijk AJ, Ruperti B, Palme K (2004) Small GTPases in vesicle trafficking. Curr Opin Plant Biol 7:694–700

    Article  CAS  PubMed  Google Scholar 

  • Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, Sugimoto K, Okabe K, Kajiwara H, Satoh K, Yamamoto K, Hirochika H, Kikuchi S (2002) Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol 130:1152–1161

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ning DL, Lu TC, Liu GF, Yang CP, Wang BC (2013) Proteomic Analysis Points to a Role for RAD23 in Apical Dominance in Pinus sylvestris var. Mongolica. Plant Mol Biol Rep 31:1283–1292

    Article  CAS  Google Scholar 

  • Nodzon LA, Xu WH, Wang Y, Pi LY, Chakrabarty PK, Song WY (2004) The ubiquitin ligase XBAT32 regulates lateral root development in Arabidopsis. Plant J 40:996–1006

    Article  CAS  PubMed  Google Scholar 

  • Petrásek J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–918

    Article  PubMed  Google Scholar 

  • Prusinkiewicz P, Crawford S, Smith RS, Ljung K, Bennett T, Ongaro V, Leyser O (2009) Control of bud activation by an auxin transport switch. Proc Natl Acad Sci USA 106(41):17431–17436

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sachs T, Thimann K (1967) The role of auxins and cytokinins in the release of buds from dominance. Am J Bot 54:136–144

    Article  CAS  Google Scholar 

  • Shimizu-Sato S, Tanaka M, Mori H (2009) Auxin-cytokinin interactions in the control of shoot branching. Plant Mol Biol 69(4):429–435

    Article  CAS  PubMed  Google Scholar 

  • Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11(1):e1001474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM (2006) SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 18(6):1396–1411

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Snow R (1929) The transmission of inhibition through dead stretches of stem. Ann Bot 43:261–267

    CAS  Google Scholar 

  • Song L, Shi QM, Yang XH, Xu ZH, Xue HW (2009) Membrane steroid-binding protein 1 (MSBP1) negatively regulates brassinosteroid signaling by enhancing the endocytosis of BAK1. Cell Res 19:864–876

    Article  CAS  PubMed  Google Scholar 

  • Stirnberg P, van De Sande K, Leyser HM (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141

    CAS  PubMed  Google Scholar 

  • Tanabe S, Ashikari M, Fujioka S, Takatsuto S, Yoshida S, Yano M, Yoshimura A, Kitano H, Matsuoka M, Fujisawa Y, Kato H, Iwasaki Y (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17:776–790

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tanaka M, Takei K, Kojima M, Sakakibara H, Mori H (2006) Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J 45:1028–1036

    Article  CAS  PubMed  Google Scholar 

  • Tong H, Chu C (2012) Brassinosteroid Signaling and Application in Rice. J Genet Genomics 39(1):3–9

    Article  CAS  PubMed  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  CAS  PubMed  Google Scholar 

  • Vieten A, Vanneste S, Wisniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Frim J (2005) Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development 132:4521–4531

    Article  CAS  PubMed  Google Scholar 

  • Wang YH, Li JY (2005) The plant architecture of rice (Oryza sativa). Plant Mol Biol 59:75–84

    Article  CAS  PubMed  Google Scholar 

  • Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Frim J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883

    Article  PubMed  Google Scholar 

  • Wu CY, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Wan J, Zhai H, Takatsuto S, Matsumoto S, Fujioka S, Feldmann KA, Pennell RI (2008) Brassinosteroids regulate grain filling in rice. Plant Cell 20:2130–2145

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yan JX, Wait R, Berkelman T, Harry RA, Westbrook JA, Wheeler CH, Dunn MJ (2000) A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 21:3666–3672

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Li G, Fang J, Chen W, Jiang H, Zou J, Liu X, Zhao X, Li X, Chu C, Xie Q, Jiang X, Zhu L (2010) The interactions among DWARF10, auxin and cytokinin underlie lateral bud outgrowth in rice. J Integr Plant Biol 52(7):626–638

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Ministry of National Science and Technology of China (Project No. 31371569), and the National Natural Science Foundation of China (Project No. 31071364).

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Authors and Affiliations

  1. Agronomy College, Nanjing Agricultural University, Nanjing, 210095, China

    Junxu Xu, Chengqiang Ding, Yanfeng Ding, She Tang, Manrong Zha, Baojie Luo & Shaohua Wang

  2. Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, Nanjing, 210095, China

    Junxu Xu, Chengqiang Ding, Yanfeng Ding, She Tang, Manrong Zha, Baojie Luo & Shaohua Wang

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  1. Junxu Xu
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Correspondence to Shaohua Wang.

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Xu, J., Ding, C., Ding, Y. et al. A Proteomic Approach to Analyze Differential Regulation of Proteins During Bud Outgrowth Under Apical Dominance Based on the Auxin Transport Canalization Model in Rice (Oryza sativa L.). J Plant Growth Regul 34, 122–136 (2015). https://doi.org/10.1007/s00344-014-9450-0

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