Abstract
Smallholder rice cultivation productivity is directly related to alleviating hunger and poverty. Biotic and abiotic stresses increasingly subvert the process, and drought is the most common stress. A mechanistic understanding of plant response to drought could lead to the use of gene-based markers to generate drought-tolerant rice. Such an understanding is challenging due to the complex interplay of genes, proteins, and metabolites. However, comparison between a wild type and its near-isogenic line (NIL) for a validated QTL can reduce noise in the omics studies and highlight critical networks and mechanisms. We compared the quantitative proteome of the flag leaves, spikelets, and roots between an upland rice genotype Vandana and its NIL 481-B. The latter contained the same genetic background as Vandana except for the QTL qDTY 12.1 for rice yield under drought. Differentially expressed proteins (DEPs) under drought were identified using isobaric labeling approach and MapMan-based analysis. DEPs were involved in photosynthesis, respiration, energy generation, and carbon–nitrogen acquisition/remobilization, largely through the pathways of sugars/starch and amino acid metabolism. DEPs could be related to drought-specific morpho-physiological responses of 481-B, reiterating the value of our results. Importantly, comparative proteome analysis of the three tissues highlighted tissue-specific differences of the same or similar proteins and underscored proteins, pathways, and mechanisms putatively involved in reproductive stage drought tolerance. More dependable and/or large-effect candidate genes/proteins might be obtained from similar multi-tissue proteomic analyses comparing wild-type plants and their NILs.
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References
Ahmadi A, Baker DA (2001) The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regul 35:81–91
Ali GM, Komatsu S (2006) Proteomic analysis of rice leaf sheath during drought stress. J Proteome Res 5:396–403
Bao Y, Kost B, Chua NH (2001) Reduced expression of α-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropsism. Plant J 28:145–157
Bernier J, Kumar A, Venuprasad R, Spaner D, Atlin G (2007) A large-effect QTL for grain yield under reproductive stage drought stress in upland rice. Crop Sci 47:507–518
Bernier J, Kumar A, Venuprasad V, Spaner D, Verulkar S, Mandal NP, Sinha PK, Peeraju P, Dongre PR, Mahto RN, Atlin G (2009a) Characterization of the effect of a QTL for drought resistance in rice, QTL12.1, over a range of environments in the Philippines and eastern India. Euphytica 166:207–217
Bernier J, Serraj R, Kumar A, Venuprasad R, Impa S, Gowda RPV, Oane R, Spaner D, Atlin G (2009b) The large-effect drought-resistance QTL12.1 increases water uptake in upland rice. Field Crops Res 110:139–146
Cantrell RP, Hettel GP (2004) Rice-based production systems for food security and poverty alleviation in Asia and the Pacific. In: Ngyun NV and Duffy R (eds) International rice commission newsletter. Proceedings of the FAO rice conference 53:75–84
Chapman N, Miller AJ, Lindsey K, Whalley WR (2012) Roots, water and nutrient acquisition: let’s get physical. Trends Plant Sci 17:701–710
De Carvalho MHC (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165
Doherty GJ, McMahon HT (2008) Mediation, modulation and consequences of membrane–cytoskeleton interactions. Annu Rev Biophys 37:65–95
Dong CH, Xia GX, Hong Y, Ramachandran S, Kost B, Chua NH (2001) ADF proteins are involved in the control of flowering and regulate F-actin organization, cell expansion, and organ growth in Arabidopsis. Plant Cell 13:1333–1346
Flexas J, Medrano H (2002) Drought inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189
Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signaling. J Exp Bot 58:2339–2358
Giani S, Breviario D (1996) Rice β-tubulins mRNA levels are modulated during flower development and in response to external stimuli. Plant Sci 116:147–157
Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730
He D, Han C, Yao J, Shen S, Yang P (2011) Constructing the metabolic and regulatory pathways in germinating rice seeds through proteomic approach. Proteomics 11:2693–2713
Henry A, Dixit S, Mandal NP, Anantha MS, Torres R, Kumar A (2014) Grain yield and physiological traits of rice lines with the drought QTL qDTY 12.1 showed different responses to drought and soil characteristics in upland environments. Funct Plant Biol 41:1066–1067
Hussey PJ, Ketelaar T, Deeks MJ (2006) Control of the actin cytoskeleton in plant cell growth. Annu Rev Plant Bio 57:109–125
Jagadish SVK, Septiningsih EM, Kohli A, Thomson MJ, Ye C, Redoña E, Kumar A, Gregorio GB, Wassmann R, Ismail AM, Singh RK (2012) Genetic advances in adapting rice to a rapidly changing climate. J Agron Crop Sci 198:360–373
Jang JC, Sheen J (1997) Sugar sensing in higher plants. Plant Cell 9:5–19
Kam MJ, Yun HS, Kaufman PB, Chang SC, Kim SK (2005) Two expansins, EXP1 and EXPB2, are correlated with the growth and development of maize roots. J Plant Biol 48:304–310
Kirch HH, Schlingensiepen S, Kotchoni S, Sunkar R, Bartels D (2005) Detailed expression analysis of selected genes of the aldehyde dehydrogenase (ALDH) gene superfamily in Arabidopsis thaliana. Plant Mol Biol 57:315–332
Kohli A, Narciso JO, Miro B, Raorane M (2012) Root proteases reinforced links between nitrogen uptake and mobilization and drought tolerance. Physiol Plant 145:165–179
Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. J Exp Bot. doi:10.1093/jxb/eru363
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lee DG, Ahsan N, Lee SH, Kang KY (2007) A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics 7:3369–3383
Lemichez E, Wu Y, Sanchez J-P, Mettouchi A, Mathur J, Chua N-H (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 15:1808–1816
Masclaux-Daubresse C, Reisdorf-Cren M, Orsel M (2008) Leaf nitrogen remobilisation for plant development and grain filling. Plant Biol 10:23–36
Meyer Y, Verdoucq L, Vignols F (1999) Plant thioredoxins and glutaredoxins: identity and putative roles. Trends Plant Sci 4:1360–1385
Milla MMAR, Maurer A, Rodriguez HA, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36:602–615
Minhas D, Grover A (1999) Transcript levels of genes encoding various genotypic and fermentation enzymes change in response to abiotic stresses. Plant Sci 146:41–51
Mishra KK, Vikram P, Yadaw RB, Swamy BPM, Dixit S, Sta Cruz MT, Maturan P, Marker S, Kumar A (2013) qDTY12.1: a locus with a consistent effect on grain yield under drought in rice. BMC Genet 14:12
O’Toole JC (1982) Adaptation of rice to drought prone environments. Drought resistance in crops with emphasis on rice. Los Baños, Laguna, pp 195–213
Oguchi K, Tanaka N, Setsuko K, Akao S (2004) Methylmalonate-semialdehyde dehydrogenase is induced in auxin-stimulated and zinc-stimulated root formation in rice. Plant Cell Rep 22:848–858
Oliver SN, Tiessen A, Fernie AR, Geigenberger P (2008) Decreased expression of plastidial adenylate kinase in potato tubers results in an enhanced rate of respiration and a stimulation of starch synthesis that is attributable to post-translational redox-activation of ADP-glucose pyrophosphorylase. J Exp Bot 59:315–325
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400
Peng Z, Wang YMC, Li F, Lv H, Cuiling Li, Xia G (2009) A proteomics study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 8:2676–2686
Perozich J, Nicholas HB, Wang BC, Lindahl R, Hempel J (1999) Relationships within the aldehyde dehydrogenase extended family. Protein Sci 8:137–146
Raorane ML, Pabuayon IM, Miro B, Kalladan R, Reza-Hazirezai M, Oane RH, Kumar A, Sreenivasulu N, Henry A, Kohli A (2015) Variation in primary metabolites in parental and near-isogenic lines of the QTL qDTY 12.1 : altered roots and flag leaves but similar spikelets of rice under drought. doi:10.1007/s11032-015-0322-5
Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151
Robredo A, Pérez-López U, Miranda-Apodaca J, Lacuesta M, Mena-Petite A, Munoz-Rueda A (2011) Elevated CO2 reduces the drought effect on nitrogen metabolism in barley plants during drought and subsequent recovery. Environ Exp Bot 71:399–408
Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J (2002) Proteomics analysis of rice leaves during drought stress and recovery. Proteomics 2:1131–1145
Serraj R, McNally KL, Slamet-Loedin I, Kohli A, Haefele SM, Atlin G, Kumar A (2011) Drought resistance improvement in rice: an integrated genetic and resource management strategy. Plant Prod Sci 14:1–14
Sheoran IS, Koonjul P, Attieh J, Saini HS (2014) Water-stress-induced inhibition of α-tubulin gene expression during growth, and its implication for reproductive success in rice. Plant Physiol Biochem 80:291–299
Smith AM, Denyer K, Martin C (1997) The synthesis of the starch granule. Annu Rev Plant Phys 48:67–87
Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98
Suralta RR (2010) Plastic root system development responses to drought-enhanced nitrogen uptake during progressive soil drying conditions in rice. Philipp Agric Sci 93:458–462
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 37:914–939
Tiessen A, Hendriks JHM, Stitt M, Brasncheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–2213
Tran LS, Nakashima K, Shinozaki K, Yamaguchi Shinozaki K (2007) Plant gene networks in osmotic stress response: from genes to regulatory networks. Methods Enzymol 428:109–128
Turyagyenda LF, Kizito EB, Ferguson M, Baguma Y, Agaba M, Harvey JJW, Osiru DSO (2013) Physiological and molecular characterization of drought responses and identification of candidate tolerance genes in cassava. AoB Plants. doi:10.1093/aobpla/plt007
Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M (2005) Water deficits affect caffeate o-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 137:949–960
Wu Y, Thorne ET, Sharp RE, Cosgrove DJ (2001) Modification of expansin transcript levels in the maize primary root at low water potentials. Plant Physiol 126:1471–1479
Zhang X, Li J, Liu A, Zou J, Zhou X, Xiang J, Rerksiri W, Peng Y, Xiong X, Chen X (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS One. doi:10.1371/journal.pone.0049652
Zhiming Y, Bo K, XiaoWei H, ShaoLei L, YouHuang B, WoNa D, Ming C, Hyung-Taeg C, Ping W (2011) Root hair-specific expansins modulate root hair elongation in rice. Plant J 66:725–734
Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310
Acknowledgments
We thank the drought physiology and breeding group for technical and field support. Funding support from the German Federal Ministry for Economic Cooperation and Development (GIZ Project 10.7860.9-001.00) and from the ‘Stress Tolerant Rice for Africa and South Asia’ (STRASA) project of the Bill and Melinda Gates Foundation is greatly appreciated.
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The authors declare that they have no competing interests.
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Raorane, M.L., Pabuayon, I.M., Varadarajan, A.R. et al. Proteomic insights into the role of the large-effect QTL qDTY 12.1 for rice yield under drought. Mol Breeding 35, 139 (2015). https://doi.org/10.1007/s11032-015-0321-6
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DOI: https://doi.org/10.1007/s11032-015-0321-6