Skip to main content
SpringerLink
Log in

Differential proteomic analysis of rice seedlings reveals the advantage of dry-raising nursery practices

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Dry-raising rice seedlings in nurseries is a key technique in high-yield rice cultivation. The present study of morphological and physiological indexes showed dry-raised seedlings (DRS) had a shorter stature, more developed root systems, and significantly higher soluble sugar, starch, and N content than moist-raised seedlings (MRS), resulting in significantly increased grain yield. Compared to the MRS techniques, the dry-raised measures induced higher levels of abscisic acid (ABA), gibberellins (GA3), and indole-3-acetic acid (IAA) in leaves and roots of seedlings. We then utilized tandem mass tags (TMT) quantitative proteomics technology to analyze the mechanism by which rice exposed to the appropriate drought stress (dry-raised measures) during the seedling stage develop differently. Through mass spectrometry, we identified 281 significantly expressed proteins in roots and 268 in leaves. The differentially expressed proteins were then divided into 23 categories based on MapMan ontology. In addition, the hormonal-related protein expression patterns of DRS were confirmed with RT-PCR at the transcript level. On the basis of these findings, we proposed that appropriate drought stress during the rice seedling stage can change the expression of key proteins involved in nitrogen uptake and translocation, hormone synthesis, photosynthesis, and CHO metabolic processes, thus regulating rice seedling growth. In this process, the differentially expressed key proteins, such as the 14-3-3 protein, GTP-binding protein, and calcium, play important roles in transduction of signals regarding soil drought, and the upregulated heat shock protein, glutathione S-transferases, and peroxidases function in enhancing the stress tolerance of the seedlings under dry-raising nursery conditions. This study established the high yielding mechanism of dry-raised cultivates methods during seedling stage at the protein expression level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

TMT:

Tandem mass tags

HPLC:

High-performance liquid chromatography

DRS:

Dry-raising seedlings

MRS:

Moist-raising seedlings

TCA:

Tricarboxylic acid cycle

NR1:

Nitrate reductase 1

NiR:

Nitrite reductase

GS:

Glutamine synthetase

GSRI2:

Glutamine synthetase root isozyme 2

ABA:

Abscisic acid

GA3:

Gibberellins

IAA:

Indole-3-acetic acid

JA:

Jasmonate

HSP:

Heat shock proteins

GST:

Glutathione S transferases

TEAB:

Triethylammonium bicarbonate

RT:

Room temperature

MS:

Mass spectrometer

RAP-DB:

Rice Genome Annotation Project database

GOGAT:

Glutamate synthase

AAO:

Abscisic aldehyde oxidase

CCD1:

Carotenoid cleavage dioxygenase 1

ILL1:

IAA-Amino acid hydrolase ILR1

GA20OX2:

Gibberellin 20 oxidase 2

LOX2.3:

Lipoxygenase 2.3

AOC 4:

Allene oxide cyclase 4

ACCO:

1-Aminocyclopropane-1-carboxylate oxidase

OPR2:

12-Oxophytodienoate reductase 2

References

  • Burger JC, Chapman MA, Burke JM (2008) Molecular insights into the evolution of crop plants. Am J Bot 95(2):113–122

    Article  PubMed  Google Scholar 

  • Campo S, Peris-Peris C, Montesinos L, Peñas G, Messeguer J, San Segundo B (2012) Expression of the maize ZmGF14-6 gene in rice confers tolerance to drought stress while enhancing susceptibility to pathogen infection. J Exp Bot 63(2):983–999

    Article  CAS  PubMed  Google Scholar 

  • Chauvin A, Caldelari D, Wolfender JL, Farmer EE (2013) Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol 197(2):566–575

    Article  CAS  PubMed  Google Scholar 

  • Chen YP, Yang WY (2005) Determination of GA3, IAA, ABA and ZT in dormant buds of Allium ovalifolium by HPLC. J Sichuan Agric Univ 23:498–500

    Google Scholar 

  • Chen F, Li Q, Sun L, He Z (2006) The rice 14-3-3 gene family and its involvement in responses to biotic and abiotic stress. DNA Res 13(16766513):53–63

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Liang Y, Lin W, Zheng L, Liang K (2007) Quality and physiobiochemical characteristics of the first rice crop seedlings under different raising seedling patterns for early rice and its ratoonal crop (I)—studies on super high-yield ecophysiology and its regulation technology in hybridize rice. Chin Agric Sci Bull 23(2):247–250

    Google Scholar 

  • Comparot S, Lingiah G, Martin T (2003) Function and specificity of 14-3-3 proteins in the regulation of carbohydrate and nitrogen metabolism. J Exp Bot 54(382):595–604

    Article  CAS  PubMed  Google Scholar 

  • Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized ppb-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26(12):1367–1372

    Article  CAS  PubMed  Google Scholar 

  • Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92(10):4114–4119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Del Viso F, Casaretto JA, Quatrano RS (2007) 14-3-3 Proteins are components of the transcription complex of the ATEM1 promoter in Arabidopsis. Planta 227(1):167–175

    Article  PubMed  Google Scholar 

  • Deryng D, Conway D, Ramankutty N, Price J, Warren R (2014) Global crop yield response to extreme heat stress under multiple climate change futures. Environ Res Lett 9(3):034011

    Article  Google Scholar 

  • Ding Y, Wang Q, Wang S, Huang P (2001) Comparison studies of roots physiology activity between rice dry seedbed seedlings and wet seedbed seedlings. J Nangjing Agric Univ 24(3):1–5

    Google Scholar 

  • Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127(7):1309–1321

    Article  CAS  PubMed  Google Scholar 

  • Dong JG, Fernandez-Maculet JC, Yang SF (1992) Purification and characterization of 1-aminocyclopropane-1-carboxylate oxidase from apple fruit. Proc Natl Acad Sci USA 89(20):9789–9793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • El-Sharkawy I, Mila I, Bouzayen M, Jayasankar S (2010) Regulation of two germinlike protein genes during plum fruit development. J Exp Bot 61(6):1761–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Y, Wu J, Lv B, Li J, Gao Z, Xu W, Baluska F, Shi W, Shaw PC, Zhang J (2015) Involvement of 14-3-3 protein GRF9 in root growth and response under polyethylene glycol-induced water stress. J Exp Bot 66(8):2271–2281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147(3):806–816

    Article  CAS  PubMed  Google Scholar 

  • Ji W, Zhu Y, Li Y, Yang L, Zhao X, Cai H, Bai X (2010) Over-expression of a glutathione S-transferase gene, GsGST, from wild soybean (Glycine soja) enhances drought and salt tolerance in transgenic tobacco. Biotechnol Lett 32(8):1173–1179

    Article  CAS  PubMed  Google Scholar 

  • Koda Y (1992) The role of jasmonic acid and related compounds in the regulation of plant development. Int Rev Cytol 135:155–199

    Article  CAS  PubMed  Google Scholar 

  • LeClere S, Tellez R, Rampey RA, Matsuda SP, Bartel B (2002) Characterization of a family of IAA-amino acid conjugate hydrolases from Arabidopsis. J Biol Chem 277(23):20446–20452

    Article  CAS  PubMed  Google Scholar 

  • Lima L, Seabra A, Melo P, Cullimore J, Carvalho H (2006) Post-translational regulation of cytosolic glutamine synthetase of Medicago truncatula. J Exp Bot 57(11):2751–2761

    Article  CAS  PubMed  Google Scholar 

  • Lin W, Wang S, Liang Y, Guo Y, He S, Hong L, Zheng L, Weng D, Pang Z (1997) Physioecological study on highyielding cultivation of rice by dryraising seedling and thinspacing transplanting techniques I. Quality and ecophysiological characteristics of rice seedlings grown on dryfertile nursery. Chin J Appl Ecol 8(6):566–570

    Google Scholar 

  • Lin W, Wang S, Liang Y, Guo Y, He S, Zheng F, Weng D, Hong L, Pan Z (1998) Physio-ecological study on high yielding cultivation of rice by dry raising seedling and thin spacing transplanting techniques II. High yielding formation and its physiobiochemical properties of early rice. Chin J Appl Ecol 9(4):395–399

    Google Scholar 

  • Lo S-F, Yang SY, Chen KT, Hsing YI, Zeevaart JA, Chen LJ, Yu SM (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20(10):2603–2618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu X, Peng L, Tang X, Liu X, Luo Z (1995) Studies on physiological reason for cold resistance of early rice seedlings raised in dry nursery. J Hunan Agric Univ 22(3):225–230

    Google Scholar 

  • Lu X, Tang X, Peng L, Liu X, Zheng X, Luo Z (1996) The characteristics of morphology, physiology and biochemistry of late rice plants cultivated by raising seedlings with dry nursery management. J Hunan Agric Univ 23(4):307–315

    Google Scholar 

  • Lu X, Peng L, Tang X, Liu X, Luo Z (1997) Studies on the morphology, tissue structure and physiological characteristics of early rice (Oryza sativa L.) seedlings raised in dry nursery. Acta Agron Sin 23(3):360–369

    Google Scholar 

  • Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annu Rev Plant Biol 47:127–158

    Article  CAS  Google Scholar 

  • Mishra A, Salokhe V (2008) Seedling characteristics and the early growth of transplanted rice under different water regimes. Exp Agric 44(03):365–383

    Article  Google Scholar 

  • Netto AT, Campostrini E, de Oliveira JG, Bressan-Smith RE (2005) Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Sci Hortic 104(2):199–209

    Article  Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16(5):553–560

    Article  CAS  PubMed  Google Scholar 

  • Ramachandra RA, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161(11):1189–1202

    Article  Google Scholar 

  • Redona E, Mackill D (1996) Genetic variation for seedling vigor traits in rice. Crop Sci 36(2):285–290

    Article  Google Scholar 

  • Schaller F, Biesgen C, Mussig C, Altmann T, Weiler EW (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210(6):979–984

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Tan BC, McCarty DR, Welch W, Zeevaart JA (2003) Substrate specificity and kinetics for VP14, a carotenoid cleavage dioxygenase in the ABA biosynthetic pathway. BBA-Biomembr 1619(1):9–14

    CAS  Google Scholar 

  • Sehnke PC, Chung HJ, Wu K, Ferl RJ (2001) Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc Natl Acad Sci USA 98(2):765–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo M, Peeters AJ, Koiwai H, Oritani T, Marion-Poll A, Zeevaart JA, Koornneef M, Kamiya Y, Koshiba T (2000) The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Acad Sci USA 97(23):12908–12913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53(366):33–37

    Article  CAS  PubMed  Google Scholar 

  • Sinclair T, Horie T (1989) Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop sci 29(1):90–98

    Article  Google Scholar 

  • Solaiman M, Hirata H (1997) Effect of arbuscular mycorrhizal fungi inoculation of rice seedlings at the nursery stage upon performance in the paddy field and greenhouse. Plant Soil 191(1):1–12

    Article  CAS  Google Scholar 

  • Stenzel I, Hause B, Miersch O, Kurz T, Maucher H, Weichert H, Ziegler J, Feussner I, Wasternack C (2003) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51(6):895–911

    Article  CAS  PubMed  Google Scholar 

  • Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939

    Article  CAS  PubMed  Google Scholar 

  • Van de Poel B, Smet D, Van Der Straeten D (2015) Ethylene and hormonal cross talk in vegetative growth and development. Plant Physiol 169(1):61–72

    Article  PubMed  PubMed Central  Google Scholar 

  • Voss I, Sunil B, Scheibe R, Raghavendra A (2013) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biol 15(4):713–722

    Article  CAS  PubMed  Google Scholar 

  • Walker BJ, VanLoocke A, Bernacchi CJ, Ort DR (2016) The costs of photorespiration to food production now and in the future. Annu Rev Plant Biol 67:107–129

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Lin W (1999) The mechanism of high-yielding in rice under dry-raising and thin-planting and its regulating technique I. Advances in the mechanism of high-yielding in rice under dry-raising and thin-planting and its prospects. J Fujian Agric Univ 28(1):12–17

    Google Scholar 

  • Wang Q, Ding Y, Wang S, Huang P, Miao B (2003) Physiological effects of sustainable water saturation in seedbed on rice dry nursery seedlings. Acta Agron Sin 30(3):210–214

    CAS  Google Scholar 

  • Wen H, Zhao J, Zhao W, Mao G (2000) Rooting advantage of rice seedlings nursed by dry-nursing and its impact on characteristics of growth and development of aerial part. J Zhejiang Agric Sci 1:1–5

    Article  Google Scholar 

  • Yang D, Duang Z, Hang J, Liu C, Wu S (2000) Study on the growth and development characters of dry nursery seedlings and their regularities of yield formation in hybrid early rice III. Characteristics of tillering and earing of dry nursery seedlings. Hubei Agric Sci 6:13–14

    CAS  Google Scholar 

  • Yao Y, Du Y, Jiang L, Liu JY (2007) I Interaction between ACC synthase 1 and 14–3-3 proteins in rice: a new insight. Biochemistry 72(9):1003–1007

    CAS  PubMed  Google Scholar 

  • Zhang Z, Qu W (2003) Guidance of plant physiology experiments, 3rd edn. Higher Education Press, Beijing. pp 127–132

  • Zhang Y, Wu H, Wang Z, Xiong F, Xie Y, Li A (1999) Effect of rice seedling raising conditions on rice seedling growth. Chinese J Rice Sci 13(2):86–90

    Google Scholar 

  • Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97(1):111–119

    Article  Google Scholar 

  • Zhang Z, Zhang Y, Liu X, Li Z, Lin W (2017) The use of comparative quantitative proteomics analysis in rice grain-filling in determining response to moderate soil drying stress. Plant Growth Regul 82(2):219–232

    Article  CAS  Google Scholar 

  • Zhao Y, Ding Y, Chen L, Huang P (2001) Physiological characteristics of drought resistance of rice dry nursery seedlings. Sci Agric Sin 34(3):289–291

    Google Scholar 

  • Zhou Q, Chen G, Chen L, Wang J, Zhang C, Lu C (2004) Study on antioxidation system in high yield hybrid rice Langyoupeijiu seedlings under dry raising conditions. Bull Bot Res 25(1):80–88

    Google Scholar 

Download references

Acknowledgements

This work was sponsored by the National Natural Science Foundation of China (No. 31401306), the Fujian-Taiwan Joint Innovative Centre for Germplasm Resources and cultivation of crop (Fujian 2011 Program, No. 2015-75), the National Key Research and Development Program of China (2016YFD0300508) and the Natural Foundation of Fujian Higher Education Institutions for Young Scientists (Key Project) (JZ160435).

Author information

Authors and Affiliations

  1. Fujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, People’s Republic of China

    Zhixing Zhang, Fenglian Huang, Hongfei Chen & Wenxiong Lin

  2. Key Laboratory of Crop Ecology and Molecular Physiology (Fujian Agriculture and Forestry University), Fujian Province University, Fuzhou, 35002, People’s Republic of China

    Zhixing Zhang, Fenglian Huang, Hongfei Chen & Wenxiong Lin

  3. Soil and Fertilizer & Resources and Environment Institute, Jiangxi Academy of Agricultural Sciences, Nanchang, 330200, People’s Republic of China

    CaiHong Shao

Authors
  1. Zhixing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fenglian Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. CaiHong Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hongfei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenxiong Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenxiong Lin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1: The RT-PCR primer of hormonal-related genes. (DOCX 19 KB)

Table S2: Effects of different seedling-raising ways on rice grain yield and its components. (DOCX 14 KB)

10725_2017_347_MOESM3_ESM.xlsx

The detailed information of the 2918 root proteins from the Rice Genome Annotation Project database (RAP-DB). (XLSX 302 KB)

10725_2017_347_MOESM4_ESM.xlsx

The detailed information of the 2674 leaf proteins from the Rice Genome Annotation Project database (RAP-DB). (XLSX 308 KB)

Functional categories of the 281 root proteins according to MapMan ontology (XLS 93 KB)

Functional categories of the 268 leaf proteins according to MapMan ontology (XLSX 29 KB)

10725_2017_347_MOESM7_ESM.docx

Figure S1: MapMan overview of leaf photosynthesis proteins with significant differences in abundance in dry-raised seedlings. (DOCX 1502 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Z., Huang, F., Shao, C. et al. Differential proteomic analysis of rice seedlings reveals the advantage of dry-raising nursery practices. Plant Growth Regul 84, 359–371 (2018). https://doi.org/10.1007/s10725-017-0347-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0347-3

Keywords

Search

Navigation