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Proteomic Analysis of Shoot Tips from Two Alfalfa Cultivars with Different Florescence

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Abstract

Flowering is an indispensable biological process for the complete life cycle of angiosperms, crucial to the regeneration of plants and the continuation of species. In this work, a proteomic approach was applied to investigate differences in protein expression in two alfalfa cultivars with different flowering periods. Shoot tips (containing bud) were collected simultaneously at the bud stage from early flowering (FF) and late flowering (MF) cultivar alfalfa. In total, 442 differentially accumulated proteins were identified, including 230 down-regulated and 212 up-regulated proteins. The identified proteins were mainly involved in metabolism, biosynthetic processes, the immune system, and responses to stimulus and translation and programmed cell death (PCD). The expression profiles demonstrated that the ubiquitin protease pathway and inositol phospholipid signaling pathway are involved in flower development regulation. Furthermore, the transcript-expression patterns of the coding proteins were consistent with the proteomic results of the increased synthesis of amino acids associated with floral organ development and involvement of Sec14p-like phosphatidylinositol transfer family protein and RAB GTPase-like protein A5D, in accordance with early pollen development. The current study is devoted to exploration of protein expression profiles during alfalfa flower development, which would be conducive to illuminate the underlying molecular mechanisms during the alfalfa flowering process. These results may provide further insights into the potential strategies for artificially controlling flowering time in alfalfa.

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References

  • Aloisi I, Cai G, Serafini-Fracassini D, Del Duca S (2016) Polyamines in pollen: from microsporogenesis to fertilization. Front Plant Sci 7(e46907):155

    PubMed  PubMed Central  Google Scholar 

  • Abdallah C, Sergeant K, Guillier C, Dumas-Gaudot E, Leclercq CC, Renaut J (2012) Optimization of i’TRAQ labelling coupled to OFFGEL fractionation as a proteomic workflow to the analysis of microsomal proteins of Medicago truncatula roots. Proteome Sci 10(1):37

    Article  CAS  Google Scholar 

  • Aribaud M, Martin TJ (1994) Polyamine metabolism, floral initiation and floral development in Chrysanthemum (Chrysanthemum morifolium Ramat.). Plant Growth Regul 15(1):23–31

    Article  CAS  Google Scholar 

  • Azevedo RA, Lancien M, Lea PJ (2006) The aspartic acid metabolic pathway, an exciting and essential pathway in plants. Amino Acids 30:143–162

    Article  CAS  Google Scholar 

  • Barnhart S (2009) Fall cutting management for alfalfa. Integrated Crop Management News. http://lib.dr.iastate.edu/cropnews

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18

    Article  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  Google Scholar 

  • Chao Y, Yang Q, Kang J, Zhang T, Sun Y (2013) Expression of the alfalfa FRIGIDA-Like gene, MsFRI-L delays flowering time in transgenic Arabidopsis thaliana. Mol Biol Rep 40:2083–2090

    Article  CAS  Google Scholar 

  • Chao Y, Zhang T, Yang Q, Kang J, Sun Y, Gruber MY (2014) Expression of the alfalfa CCCH-type zinc finger protein gene MsZFN delays flowering time in transgenic Arabidopsis thaliana. Plant Sci 215-216(3):92–99

    Article  CAS  Google Scholar 

  • Chen L, Chen Q, Zhu Y, Hou L, Mao P (2016) Proteomic identification of differentially expressed proteins during alfalfa (Medicago sativa L.) flower development. Front Plant Sci 7

  • Coe EH, Mccormick SM, Modena SA (1981) White pollen in maize. J Hered 72:318–320

    Article  Google Scholar 

  • Conesa A, Götz S (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832

    Article  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    Article  CAS  Google Scholar 

  • de Graaf BHJ (2005) Rab11 GTPase-regulated membrane trafficking is crucial for tip-focused pollen tube growth in tobacco. Plant Cell Online 17:2564–2579

    Article  Google Scholar 

  • Gagne JM, Downes BP, Shiu SH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA 99(17):11519–11524

    Article  CAS  Google Scholar 

  • Gao R, Gruber MY, Amyot L, Hannoufa A (2018) SPL13 regulates shoot branching and flowering time in Medicago sativa. Plant Mol Biol 96:119–133

    Article  CAS  Google Scholar 

  • Gong F, Wu X, Wang W (2015) Diversity and function of maize pollen coat proteins: from biochemistry to proteomics. Front Plant Sci 6:199

    PubMed  PubMed Central  Google Scholar 

  • Gupta ML, Macmillan RH, Gupta ML, Macmillan RH, Mcmahon TA, Bennett DW (2010) A simulation model to predict the drying time for pasture hay. Grass Forage Sci 44(1):1–10

    Article  Google Scholar 

  • Han L, Mason M, Risseeuw EP, Crosby WL, Somers DE (2010) Formation of an SCFZTL complex is required for proper regulation of circadian timing. Plant J 40:291–301

    Article  Google Scholar 

  • Hayama R, Coupland G (2003) Shedding light on the circadian clock and the photoperiodic control of flowering. Curr Opin Plant Biol 6:13–19

    Article  CAS  Google Scholar 

  • Hayward MD, Mcadam NJ (2010) The effect of isozyme selection on yield and flowering time in Lolium perenne. Plant Breed 101:24–29

    Article  Google Scholar 

  • Heller W, Forkmann G (1993) Biosynthesis of Flavonoids. In: Harborne JB (ed) The flavonoids: advances in research Since 1986. Chapman and Hall, London, pp. 499–535.

    Chapter  Google Scholar 

  • Hershko A, Ciechanover A, Varshavsky A (2000) The ubiquitin system. Annu Rev Biochem 67:425–479

    Article  Google Scholar 

  • Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16:S1

    Article  CAS  Google Scholar 

  • Johnson ET, Ryu S, Yi H, Shin B, Cheong H, Choi G (2010) Alteration of a single amino acid changes the substrate specificity of dihydroflavonol 4-reductase. Plant J 25:325–333

    Article  Google Scholar 

  • Kanehisa M (2000) Post-genome informatics. Oxford University Press

  • Kim HJ, Ok SH, Bahn SC, Jang J, Oh SA, Park SK, Twell D, Ryu SB, Shin JS (2011) Endoplasmic reticulum- and Golgi-localized phospholipase A2 plays critical roles in Arabidopsis pollen development and germination. Plant Cell 23:94–110

    Article  CAS  Google Scholar 

  • Koepp DM, Harper JW, Elledge SJ (1999) How the cyclin became a cyclin: regulated proteolysis in the cell cycle. Cell 97:431–434

    Article  CAS  Google Scholar 

  • Komeda Y (2004) Genetic regulation of time to flower in Arabidopsis thaliana. Annu Rev Plant Biol 55:521–535

    Article  CAS  Google Scholar 

  • Koornneef M, Hanhart CJ, Veen JHVD (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66

    Article  CAS  Google Scholar 

  • Kraus J, Menze A, Wurbs D (2011) Inhibition of bolting and flowering of a sugar beet plant. US Patent US9222102B2

  • Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698

    Article  CAS  Google Scholar 

  • Lawton-Rauh AL, Alvarez-Buylla ER, Purugganan MD (2000) Molecular evolution of flower development. Trends Ecol Evol 15:144–149

    Article  CAS  Google Scholar 

  • Lu D, Ni W, Stanley BA, Ma H (2016) Proteomics and transcriptomics analyses of Arabidopsis floral buds uncover important functions of Arabidopsis SKP1-LIKE1. BMC Plant Biol 16:61

    Article  Google Scholar 

  • Mo Y, Nagel C, Taylor LP (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc Natl Acad Sci USA 89:7213–7217

    Article  CAS  Google Scholar 

  • Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I (2003) The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. Plant J 35:613–623

    Article  CAS  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14:S111

    Article  CAS  Google Scholar 

  • Munnik T, Vermeer JEM (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33:655–669

    Article  CAS  Google Scholar 

  • Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75:4646–4658

    Article  CAS  Google Scholar 

  • Oberg AL, Mahoney DW, Eckel-Passow JE, Malone CJ, Wolfinger RD, Hill EG, Cooper LT, Onuma OK, Spiro C, Therneau TM (2008) Statistical analysis of relative labeled mass spectrometry data from complex samples using ANOVA. J Proteome Res 7:225–233

    Article  CAS  Google Scholar 

  • Pan HC, Li JH, Wang XZ (2005) Involvement of ethylene and 1-aminocyclopropane-1-carboxylate synthase gene in regulation of programmed cell death during rose (Rosa x hybrida) flower development. Acta Photophysiologica Sinica 31:354

    CAS  Google Scholar 

  • Rahman MH, Bennett RA, Yang RC, Kebede B, Thiagarajah MR (2011) Exploitation of the late flowering species Brassica oleracea L. for the improvement of earliness in B. napus L.: an untraditional approach. Euphytica 177:365–374

    Article  Google Scholar 

  • Reeves PH, Coupland G (2000) Response of plant development to environment: control of flowering by daylength and temperature. Curr Opin Plant Biol 3:37–42

    Article  CAS  Google Scholar 

  • Samach A, Klenz JE, Kohalmi SE, Risseeuw E, Haughn GW, Crosby WL (2010) The UNUSUAL FLORAL ORGANS gene of Arabidopsis thaliana is an F-box protein required for normal patterning and growth in the floral meristem. Plant J 20:433–445

    Article  Google Scholar 

  • Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ERE, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1–Skp2complex. Nature 408:381

    Article  CAS  Google Scholar 

  • Schwechheimer C (2004) The COP9 signalosome (CSN): an evolutionary conserved proteolysis regulator in eukaryotic development. Biochim Biophys Acta 1695:45–54

    Article  CAS  Google Scholar 

  • Simon R, Igeño MI, Coupland G (1996) Activation of floral meristem identity genes in Arabidopsis. Nature 384:59–62

    Article  CAS  Google Scholar 

  • Simpson GG, Dean C (2002) Arabidopsis, the Rosetta Stone of flowering time? Science 296:285–289

    Article  CAS  Google Scholar 

  • Simpson GG, Gendall AR, Dean C (1999) When to switch to flowering. Annu Rev Cell Dev Biol 15:519–550

    Article  CAS  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stout DG (1986) The critical fall harvest period for alfalfa in interior British Columbia. Can J Plant Sci 66(3):565–578

    Article  Google Scholar 

  • Takahashi N, Kuroda H, Kuromori T, Hirayama T, Seki M, Shinozaki K, Shimada H, Matsui M (2004) Expression and interaction analysis of Arabidopsis Skp1-related genes. Plant Cell Physiol 45:83–91

    Article  CAS  Google Scholar 

  • Thiruvengadam M, Shih CF, Yang CH (2015) Expression of an antisense Brassica oleracea GIGANTEA (BoGI) gene in transgenic Broccoli causes delayed flowering, leaf senescence, and post-harvest yellowing retardation. Plant Mol Biol Report 33:1499–1509

    Article  CAS  Google Scholar 

  • Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA (2005) A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Biol 168:801–812

    Article  CAS  Google Scholar 

  • Wang C, Tian Q, Hou Z, Mucha M, Aukerman M, Olsen OA (2007) The Arabidopsis thaliana AT PRP39-1 gene, encoding a tetratricopeptide repeat protein with similarity to the yeast pre-mRNA processing protein PRP39, affects flowering time. Plant Cell Rep 26:1357–1366

    Article  CAS  Google Scholar 

  • Wang MY, Song YL, Zhang SX, Zhao XL, Wang JW, Niu N, Zhang GS (2015) Analysis of skp1 gene expression in physiological male sterility induced by chemical hybridizing agent sq-1 in wheat (Triticum aestivum L.). Cereal Res Commun 43:204–212

    Article  Google Scholar 

  • Wisniewski J, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6(5):359–362

    Article  CAS  Google Scholar 

  • Woodson WR, Park KY, Larsen PB, Wang H (1992) Expression of ethylene biosynthetic pathway transcripts in senescing Carnation flowers. Plant Physiol 99:526

    Article  CAS  Google Scholar 

  • Yang M, Hu Y, Lodhi M, Mccombie WR, Ma H (1999) The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc Natl Acad Sci USA 96:11416–11421

    Article  CAS  Google Scholar 

  • Zhang S, Yang C, Peng J, Sun S, Wang X (2009) GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol Biol 69:745–759

    Article  CAS  Google Scholar 

  • Zhang T, Chao Y, Kang J, Ding W, Yang Q (2013) Molecular cloning and characterization of a gene regulating flowering time from Alfalfa (Medicago sativa L.). Mol Biol Rep 40:4597–4603

    Article  CAS  Google Scholar 

  • Zhang X, Li Q, Zheng C (1999) Hormonal regulation of postpollination development of Doritaenopsis flowers by auxin and ethylene. Acta Photophysiol Sinica 25:178–186

    CAS  Google Scholar 

  • Zhao D, Yu Q, Chen M, Ma H (2001) The ASK1 gene regulates B function gene expression in cooperation with UFO and LEAFY in Arabidopsis. Development 128:2735

    CAS  PubMed  Google Scholar 

  • Zhao D, Han T, Risseeuw E, Crosby WL, Ma H (2003) Conservation and divergence of ASK1 and ASK2 gene functions during male meiosis in Arabidopsis thaliana. Plant Mol Biol 53:163–173

    Article  CAS  Google Scholar 

  • Zhao D, Yang X, Quan L, Timofejeva L, Rigel NW, Ma H, Makaroff CA (2006) ASK1, a SKP1 homolog, is required for nuclear reorganization, presynaptic homolog juxtaposition and the proper distribution of cohesin during meiosis in Arabidopsis. Plant Mol Biol 62:99–110

    Article  CAS  Google Scholar 

  • Zhao D, Yang M, Solava J, Ma H (2015) The ASK1 gene regulates development and interacts with the UFO gene to control floral organ identity in Arabidopsis. Genesis 25:209–223

    Google Scholar 

Download references

Acknowledgments

This work was supported by the earmarked fund for China Agriculture Research System (CARS-34), the National Key Basic Research Program of China (973 Program) (2015CB943500), and Agricultural Science and Technology Innovation Program (ASTIP-IAS14).

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  1. Hao Sun and Ruicai Long contributed equally to this work.

Authors and Affiliations

  1. Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100193, People’s Republic of China

    Hao Sun, Ruicai Long, Fan Zhang, Tiejun Zhang, Junmei Kang, Zhen Wang, Jie Yu & Qingchuan Yang

  2. Bioengineering College, Chongqing University, Chongqing, 400044, People’s Republic of China

    Chunyu Cao

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  1. Hao Sun
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  2. Ruicai Long
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Sun, H., Long, R., Zhang, F. et al. Proteomic Analysis of Shoot Tips from Two Alfalfa Cultivars with Different Florescence. Plant Mol Biol Rep 37, 265–276 (2019). https://doi.org/10.1007/s11105-019-01153-6

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