Advertisement

Amino Acids

, Volume 50, Issue 1, pp 149–161 | Cite as

Long photoperiod affects the maize transition from vegetative to reproductive stages: a proteomic comparison between photoperiod-sensitive inbred line and its recurrent parent

  • Lei Tian
  • Shunxi Wang
  • Xiaoheng Song
  • Jun Zhang
  • Ping Liu
  • Zan Chen
  • Yanhui Chen
  • Liuji Wu
Original Article

Abstract

Maize (Zea mays L.) is a typical short-day plant that is produced as an important food product and industrial material. The photoperiod is one of the most important evolutionary mechanisms enabling the adaptation of plant developmental phases to changes in climate conditions. There are differences in the photoperiod sensitivity of maize inbred lines from tropical to temperate regions. In this study, to identify the maize proteins responsive to a long photoperiod (LP), the photoperiod-insensitive inbred line HZ4 and its near-isogenic line H496, which is sensitive to LP conditions, were analyzed under long-day conditions using isobaric tags for relative and absolute quantitation. We identified 5259 proteins in maize leaves exposed to the LP condition between the vegetative and reproductive stages. These proteins included 579 and 576 differentially accumulated proteins in H496 and HZ4 leaves, respectively. The differentially accumulated proteins (e.g., membrane, defense, and energy- and ribosome-related proteins) exhibited the opposite trends in HZ4 and H496 plants during the transition from the vegetative stage to the reproductive stage. These results suggest that the photoperiod-associated fragment in H496 plants considerably influences various proteins to respond to the photoperiod sensitivity. Overall, our data provide new insights into the effects of long-day treatments on the maize proteome, and may be useful for the development of new germplasm.

Keywords

Proteomic analysis Maize leaves iTRAQ Long photoperiod Near-isogenic line Developmental processes 

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (no. 31101158), the National Basic Research Program of China (973 Program, no. 2011CB111500), and the China Postdoctoral Science Foundation (no. 20100470993).

Author contributions

Conceived and designed the experiments: YC and LW. Performed the experiments: LT, LW, XS, JZ, SW, PL, and ZC. Analyzed the data: LW, SW, and XS. Contributed reagents/materials/analysis tools: YC and SW. Wrote the manuscript: LT, LW, and YC.

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical standard

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

726_2017_2501_MOESM1_ESM.tif (100 kb)
Venn diagram of differentially accumulated proteins. (A) Proteins differentially accumulated between H496 and HZ4 plants from the three-leaf stage to the six-leaf stage. (B) Proteins differentially accumulated between the leaves and shoot apical meristems. (TIFF 99 kb)
726_2017_2501_MOESM2_ESM.tif (161 kb)
Protein accumulation pattern differences between HZ4 and H496 plants from the three-leaf stage to the six-leaf stage. (A) Venn diagram of differentially accumulated proteins identified in HZ4 and H496 shoot apical meristems (SAMs) from the three-leaf stage to the six-leaf stage. (B) Number of differentially accumulated proteins identified in HZ4 and H496 SAMs from the three-leaf stage to the six-leaf stage. (C) Number of proteins common to the HZ4 and H496 SAMs. (TIFF 160 kb)
726_2017_2501_MOESM3_ESM.tif (1 mb)
Dynamics of specific biological process proteins differentially accumulated between HZ4 and H496 plants. (A–D) Accumulation level of proteins identified in line HZ4 related to defense (A), transport (B), plant development (C), and cell development (D). (E–H) Accumulation level of proteins identified in line H496 involved in defense (E), transport (F), plant development (G), and cell development (H). (TIFF 1053 kb)
726_2017_2501_MOESM4_ESM.tif (1.5 mb)
Differences between HZ4 and H496 plants regarding the dynamic change of proteins involved in metabolic processes. (A and B) Proteins specific to HZ4 (A) or H496 (B) plants. (C) Proteins common to HZ4 and H496 plants from the three-leaf stage to the six-leaf stage. (TIFF 1517 kb)
726_2017_2501_MOESM5_ESM.xlsx (564 kb)
Supplementary material 5 (XLSX 563 kb)
726_2017_2501_MOESM6_ESM.xlsx (2.1 mb)
Supplementary material 6 (XLSX 2107 kb)
726_2017_2501_MOESM7_ESM.xlsx (72 kb)
Supplementary material 7 (XLSX 71 kb)
726_2017_2501_MOESM8_ESM.xlsx (73 kb)
Supplementary material 8 (XLSX 72 kb)
726_2017_2501_MOESM9_ESM.xlsx (75 kb)
Supplementary material 9 (XLSX 74 kb)
726_2017_2501_MOESM10_ESM.xlsx (9 kb)
Supplementary material 10 (XLSX 9 kb)

References

  1. Adams S, Carre IA (2011) Downstream of the plant circadian clock: output pathways for the control of physiology and development. Essays Biochem 49(1):53–69PubMedCrossRefGoogle Scholar
  2. Araki T (2001) Transition from vegetative to reproductive phase. Curr Opin Plant Biol 4(1):63–68PubMedCrossRefGoogle Scholar
  3. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J (2009) ClueGO: a Cytoscape plug-into decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25(8):1091–1093PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bindea G, Galon J, Mlecnik B (2013) CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data. Bioinformatics 29(5):661–663PubMedPubMedCentralCrossRefGoogle Scholar
  5. Blazquez M (2000) Flower development pathways. J Cell Sci 113(Pt 20):3547–3548PubMedGoogle Scholar
  6. Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20(10):2586–2602PubMedPubMedCentralCrossRefGoogle Scholar
  7. Choudhary MK, Nomura Y, Wang L, Nakagami H, Somers DE (2015) Quantitative circadian phosphoproteomic analysis of Arabidopsis reveals extensive clock control of key components in physiological, metabolic, and signaling pathways. Mol Cell Proteom 14(8):2243–2260CrossRefGoogle Scholar
  8. Coneva V, Guevara D, Rothstein SJ, Colasanti J (2012) Transcript and metabolite signature of maize source leaves suggests a link between transitory starch to sucrose balance and the autonomous floral transition. J Exp Bot 63(14):5079–5092PubMedPubMedCentralCrossRefGoogle Scholar
  9. Dai Z, Gao J, An K, Lee JM, Edwards GE, An G (1996) Promoter elements controlling developmental and environmental regulation of a tobacco ribosomal protein gene L34. Plant Mol Biol 32(6):1055–1065PubMedCrossRefGoogle Scholar
  10. Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309(5734):630–633PubMedCrossRefGoogle Scholar
  11. Doebley J (2004) The genetics of maize evolution. Annu Rev Genet 38:37–59PubMedCrossRefGoogle Scholar
  12. Dong Z, Danilevskaya O, Abadie T, Messina C, Coles N, Cooper M (2012) A gene regulatory network model for floral transition of the shoot apex in maize and its dynamic modeling. PLoS One 7(8):e43450PubMedPubMedCentralCrossRefGoogle Scholar
  13. Dron A, Rabouille S, Claquin P, Talec A, Raimbault V, Sciandra A (2013) Photoperiod length paces the temporal orchestration of cell cycle and carbon-nitrogen metabolism in Crocosphaera watsonii. Environ Microbiol 15(12):3292–3304PubMedCrossRefGoogle Scholar
  14. Du Y, He W, Deng C, Chen X, Gou L, Zhu F, Guo W, Zhang J, Wang T (2016) Flowering-related RING Protein 1 (FRRP1) regulates flowering time and yield potential by affecting Histone H2b monoubiquitination in rice (Oryza sativa). PLoS One 11(3):e0150458PubMedPubMedCentralCrossRefGoogle Scholar
  15. Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX, Purugganan MD (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics 183(1):325–335PubMedPubMedCentralCrossRefGoogle Scholar
  16. Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141(3):e551–e552CrossRefGoogle Scholar
  17. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci USA 107(20):9458–9463PubMedPubMedCentralCrossRefGoogle Scholar
  18. Gu X, Jiang D, Wang Y, Bachmair A, He Y (2009) Repression of the floral transition via histone H2B monoubiquitination. Plant J 57(3):522–533PubMedCrossRefGoogle Scholar
  19. Hoenicka H, Lehnhardt D, Briones V, Nilsson O, Fladung M (2016) Low temperatures are required to induce the development of fertile flowers in transgenic male and female early flowering poplar (Populus tremula L.). Tree Physiol 36(5):667–677PubMedPubMedCentralCrossRefGoogle Scholar
  20. Hung HY, Shannon LM, Tian F, Bradbury PJ, Chen C, Flint-Garcia SA, McMullen MD, Ware D, Buckler ES, Doebley JF (2012) ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA 109(28):E1913–E1921PubMedPubMedCentralCrossRefGoogle Scholar
  21. Izawa T (2012) Physiological significance of the plant circadian clock in natural field conditions. Plant Cell Environ 35(10):1729–1741PubMedCrossRefGoogle Scholar
  22. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30PubMedPubMedCentralCrossRefGoogle Scholar
  23. Kobayashi M, Takato H, Fujita K, Suzuki S (2012) HSG1, a grape Bcl-2-associated athanogene, promotes floral transition by activating CONSTANS expression in transgenic Arabidopsis plant. Mol Biol Rep 39(4):4367–4374PubMedCrossRefGoogle Scholar
  24. Ku LX, Li SY, Chen XA, Wu LC, Wang XT, Chen YH (2011) Cloning and characterization of putative Hd6 ortholog associated with Zea mays L. photoperiod sensitivity. Agric Sci China 10(1):18–27CrossRefGoogle Scholar
  25. Ku L, Tian L, Su H, Wang C, Wang X, Wu L, Shi Y, Li G, Wang Z, Wang H (2016) Dual functions of the ZmCCT-associated quantitative trait locus in flowering and stress responses under long-day conditions. BMC Plant Biol 16(1):239PubMedPubMedCentralCrossRefGoogle Scholar
  26. Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev 14(18):2366–2376PubMedPubMedCentralCrossRefGoogle Scholar
  27. Legnaioli T, Cuevas J, Mas P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28(23):3745–3757PubMedPubMedCentralCrossRefGoogle Scholar
  28. Leiboff S, DeAllie CK, Scanlon MJ (2016) Modeling the Morphometric Evolution of the Maize Shoot Apical Meristem. Front Plant Sci 7:1651PubMedPubMedCentralCrossRefGoogle Scholar
  29. Liu C, Thong Z, Yu H (2009) Coming into bloom: the specification of floral meristems. Development 136(20):3379–3391PubMedCrossRefGoogle Scholar
  30. Liu L, Zhu Y, Shen L, Yu H (2013) Emerging insights into florigen transport. Curr Opin Plant Biol 16(5):607–613PubMedCrossRefGoogle Scholar
  31. Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez GJ, Buckler E, Doebley J (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99(9):6080–6084PubMedPubMedCentralCrossRefGoogle Scholar
  32. McSteen P, Laudencia-Chingcuanco D, Colasanti J (2000) A floret by any other name: control of meristem identity in maize. Trends Plant Sci 5(2):61–66PubMedCrossRefGoogle Scholar
  33. Méchin V, Damerval C, Zivy M (2007) Total protein extraction with TCA-acetone. Methods Mol Biol 355:1–8PubMedGoogle Scholar
  34. Menard R, Verdier G, Ors M, Erhardt M, Beisson F, Shen WH (2014) Histone H2B monoubiquitination is involved in the regulation of cutin and wax composition in Arabidopsis thaliana. Plant Cell Physiol 55(2):455–466PubMedCrossRefGoogle Scholar
  35. Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23(3):942–960PubMedPubMedCentralCrossRefGoogle Scholar
  36. Nakamichi N, Kusano M, Fukushima A, Kita M, Ito S, Yamashino T, Saito K, Sakakibara H, Mizuno T (2009) Transcript profiling of an Arabidopsis PSEUDO RESPONSE REGULATOR arrhythmic triple mutant reveals a role for the circadian clock in cold stress response. Plant Cell Physiol 50(3):447–462PubMedCrossRefGoogle Scholar
  37. Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457(7227):327–331PubMedCrossRefGoogle Scholar
  38. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448(7151):358–361PubMedCrossRefGoogle Scholar
  39. Reference Genome Group of the Gene Ontology C (2009) The Gene Ontology’s Reference Genome Project: a unified framework for functional annotation across species. PLoS Comput Biol 5(7):e1000431CrossRefGoogle Scholar
  40. Riboni M, Galbiati M, Tonelli C, Conti L (2013) GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS. Plant Physiol 162(3):1706–1719PubMedPubMedCentralCrossRefGoogle Scholar
  41. Riboni M, Robustelli Test A, Galbiati M, Tonelli C, Conti L (2014) Environmental stress and flowering time: the photoperiodic connection. Plant Signal Behav 9(7):e29036PubMedCentralCrossRefGoogle Scholar
  42. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288(5471):1613–1616PubMedCrossRefGoogle Scholar
  43. Shi C, Baldwin IT, Wu J (2012) Arabidopsis plants having defects in nonsense-mediated mRNA decay factors UPF1, UPF2, and UPF3 show photoperiod-dependent phenotypes in development and stress responses. J Integr Plant Biol 54(2):99–114PubMedCrossRefGoogle Scholar
  44. Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296(5566):285–289PubMedCrossRefGoogle Scholar
  45. Steeves TA, Sussex IM (1989) Patterns in plant development, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  46. Thompson BE, Basham C, Hammond R, Ding Q, Kakrana A, Lee TF, Simon SA, Meeley R, Meyers BC, Hake S (2014) The dicer-like1 homolog fuzzy tassel is required for the regulation of meristem determinacy in the inflorescence and vegetative growth in maize. Plant Cell 26(12):4702–4717PubMedPubMedCentralCrossRefGoogle Scholar
  47. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136(6):1005–1016PubMedCrossRefGoogle Scholar
  48. Victor KJ, Fennell AY, Grimplet J (2010) Proteomic analysis of shoot tissue during photoperiod induced growth cessation in V. riparia Michx. grapevines. Proteome Sci 8:44PubMedPubMedCentralCrossRefGoogle Scholar
  49. Wang Z, Wang T (2011) Dynamic proteomic analysis reveals diurnal homeostasis of key pathways in rice leaves. Proteomics 11(2):225–238PubMedCrossRefGoogle Scholar
  50. Wang S, Carver B, Yan L (2009) Genetic loci in the photoperiod pathway interactively modulate reproductive development of winter wheat. Theor Appl Genet 118(7):1339–1349PubMedCrossRefGoogle Scholar
  51. Wisniewski ME, Bassett CL, Renaut J, Farrell R Jr, Tworkoski T, Artlip TS (2006) Differential regulation of two dehydrin genes from peach (Prunus persica) by photoperiod, low temperature and water deficit. Tree Physiol 26(5):575–584PubMedCrossRefGoogle Scholar
  52. Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6(5):359–362PubMedCrossRefGoogle Scholar
  53. Wong CE, Singh MB, Bhalla PL (2013) The dynamics of soybean leaf and shoot apical meristem transcriptome undergoing floral initiation process. PLoS One 8(6):e65319PubMedPubMedCentralCrossRefGoogle Scholar
  54. Wu LC, Wang TG, Ku LX, Huang QC, Sun ZH, Xia ZL (2008) Determination of the photoperiod-sensitive inductive phase in maize with leaf numbers and morphologies of stem apical meristem. Agric Sci China 7:554–560CrossRefGoogle Scholar
  55. Wu L, Tian L, Wang S, Zhang J, Liu P, Tian Z, Zhang H, Liu H, Chen Y (2016a) Comparative proteomic analysis of the response of maize (Zea mays L.) leaves to long photoperiod condition. Front Plant Sci 7:752PubMedPubMedCentralGoogle Scholar
  56. Wu L, Wang X, Wang S, Wu L, Tian L, Tian Z, Liu P, Chen Y (2016b) Comparative proteomic analysis of the shoot apical meristem in maize between a ZmCCT-associated near-isogenic line and its recurrent parent. Sci Rep 6:30641PubMedPubMedCentralCrossRefGoogle Scholar
  57. Xu L, Menard R, Berr A, Fuchs J, Cognat V, Meyer D, Shen WH (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J 57(2):279–288PubMedCrossRefGoogle Scholar
  58. Yadav RK, Snipes S, Girke T, Reddy GV (2013) Gene expression analysis of shoot apical meristem cell types. Methods Mol Biol 959:235–245PubMedCrossRefGoogle Scholar
  59. Yang XH, Xu ZH, Xue HW (2005) Arabidopsis membrane steroid binding protein 1 is involved in inhibition of cell elongation. Plant Cell 17(1):116–131PubMedPubMedCentralCrossRefGoogle Scholar
  60. Yang X, Song L, Xue HW (2008) Membrane steroid binding protein 1 (MSBP1) stimulates tropism by regulating vesicle trafficking and auxin redistribution. Mol Plant 1(6):1077–1087PubMedCrossRefGoogle Scholar
  61. Yang Q, Li Z, Li W, Ku L, Wang C, Ye J, Li K, Yang N, Li Y, Zhong T (2013) CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci USA 110(42):16969–16974PubMedPubMedCentralCrossRefGoogle Scholar
  62. Yanovsky MJ, Kay SA (2002) Molecular basis of seasonal time measurement in Arabidopsis. Nature 419(6904):308–312PubMedCrossRefGoogle Scholar
  63. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297PubMedPubMedCentralCrossRefGoogle Scholar
  64. Yu H, Xu Y, Tan EL, Kumar PP (2002) AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci USA 99(25):16336–16341PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria 2017

Authors and Affiliations

  • Lei Tian
    • 1
    • 2
  • Shunxi Wang
    • 1
    • 2
  • Xiaoheng Song
    • 1
    • 2
  • Jun Zhang
    • 3
  • Ping Liu
    • 1
    • 2
  • Zan Chen
    • 1
    • 2
  • Yanhui Chen
    • 1
    • 2
  • Liuji Wu
    • 1
    • 2
  1. 1.Henan Agricultural University and Synergetic Innovation Center of Henan Grain CropsZhengzhouChina
  2. 2.Key Laboratory of Physiological Ecology and Genetic Improvement of Food Crops in Henan ProvinceZhengzhouChina
  3. 3.Food Crops Research InstituteHenan Academy of Agricultural ScienceZhengzhouChina

Personalised recommendations