Abstract
Root growth in drying soil is generally limited by a combination of mechanical impedance and water stress. As the major function of root tissue is water and nutrient uptake, so it imparts an important role in plant growth and stress management. Previously, we have studied physiological performance and expression profiling of gene associated with drought tolerance in leaf tissue of four cotton varieties. Here, we have further continued our studies with the root tissue of these varieties. The Gossypium hirsutum species JKC-770 is drought-tolerant and KC-2 is drought-sensitive, while Gossypium herbaceum species JKC-717 is drought-tolerant and RAHS-187 is drought-sensitive. JKC-770 and JKC-717 the drought-tolerant varieties showed a comparatively high glutathione-S-transferase, superoxide dismutase, proline along with their gene expression, and low malondialdehyde content indicating low membrane damage and better antioxidative defense under drought condition. The expression levels of cellulose synthase, xyloglucan:xyloglucosyl transferase, and glycosyl hydrolases suggest modulation in cell wall structure and partitioning of sugars towards osmoprotectants instead of cell wall biosynthesis in tolerant varieties. Heat shock proteins and serine/threonine protein phosphotases show upregulation under drought condition, which are responsible for temperature tolerance and protein phosphorylation, respectively. These effects many metabolic processes and may be playing a key role in drought tolerance and adaptability of JKC-770 towards drought tolerance. The long-term water use efficiency (WUE) estimated in terms of carbon isotope discrimination (∆13C) in the root tissues showed maximum depletion in the ∆13C values in JKC-770 variety, while minimum in RAHS-187 under drought stress with reference to their respective control, suggesting a high WUE in JKC-770 variety.
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Abbreviations
- ∆13C:
-
carbon isotope discrimination
- ABA:
-
abscisic acid
- Aux Res P:
-
auxin responsive protein
- CesA:
-
cellulose synthase
- DW:
-
dry weight
- FW:
-
fresh weight
- GABA:
-
γ-amino butyric acid
- GAD:
-
glutamate decarboxylase
- GH:
-
glycosyl hydrolases
- GST:
-
glutathione-S-transferase
- H2O2 :
-
hydrogen peroxide
- HC:
-
hydraulic conductance
- HPFM:
-
high-pressure flow meter
- HSP:
-
heat-shock proteins
- MDA:
-
malondialdehyde
- MSTFA:
-
N-methyl-N-(trimethylsilyl) trifluoroacetamide
- NBT:
-
nitroblue tetrazolium
- PCA:
-
principal component analysis
- PPFD:
-
photosynthetic photon flux density
- ROS:
-
reactive oxygen species
- RWC:
-
relative water content
- Ser/Thr PPase:
-
serine/threonine protein phosphotases
- SOD:
-
superoxide dismutase
- SqE:
-
squalene epoxidase
- TCH4:
-
xyloglucan:xyloglucosyl transferase
- WUE:
-
water use efficiency
- Δ1P5CS:
-
Δ1-pyrroline-5-carboxylase synthetase
References
Babb VM, Haigler CH (2001) Sucrose phosphate synthase activity rises in correlation with high-rate cellulose synthesis in three heterotrophic systems. Plant Physiol 127:1234–1242
Bengough AG, McKenzie BM, Hallett PD, Valentine TA (2011) Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits. J Exp Bot 62:59–68
Beuve N, Rispail N, Laine P, Cliquet JB, Ourry A, Le Deunff E (2004) Putative role of γ‐aminobutyric acid (GABA) as a long‐distance signal in up‐regulation of nitrate uptake in Brassica napus L. Plant Cell Environ 27:1035–1046
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566
Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field. Photosynthesis and growth. Ann Bot 89:907–916
Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43:273–283
DaMatta FM, Chaves ARM, Pinheiro HA, Ducatti C, Loureiro ME (2003) Drought tolerance of two field-grown clones of Coffea canephora. Plant Sci 164:111–117
Davies WJ, Kudoyarova G, Hartung W (2005) Long-distance ABA signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the plant’s response to drought. J Plant Growth Regul 24:285–295
Evans A, DeHaven C, Barrett T, Mitchell M, Milgram E (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81:6656–6667
Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–137
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537
Foyer CH, Valadier MH, Migge A, Becker TW (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol 117:283–292
Gewin V (2010) Food: an underground revolution. Nature 466:552–553
Henry A, Cal AJ, Batoto TC, Torres RO, Serraj R (2012) Root attributes affecting water uptake of rice (Oryza sativa) under drought. J Exp Bot 63:4751–4763
Hochholdinger F, Tuberosa R (2009) Genetic and genomic dissection of maize root development and architecture. Curr Opin Plant Biol 12:172–177
Hrmova M, Farkas V, Lahnstein J, Fincher GB (2007) A barley xyloglucan xyloglucosyl transferase covalently links xyloglucan, cellulosic substrates, and (1, 3; 1, 4)-β-d-glucans. J Biol Chem 282:12951–12962
Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25
Kishor PBK, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394
Lee EJ, Matsumura Y, Soga K, Hoson T, Koizumi N (2007) Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. Plant Cell Physiol 48:405–413
Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. In: Perrot-Rechenman C and Hagen G, (eds) Auxin molecular biology. Springer, Netherlands. pp: 387–400
Manavalan LP, Guttikonda SK, Tran LSP, Nguyen HT (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50:1260–1276
Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288
Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynth Res 86:459–474
Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170
Park JK, Jin SH, Choi KH, Ko JH, Baek NI, Choi SY, Cho SW, Choi KJ, Nam KY (1999) Influence of ginsenosides on the kainic acid-induced seizure activity in immature rats. J Biochem Mol Biol 32:339–344
Piens K, Fauré R, Sundqvist G, Baumann MJ, Saura-Valls M, Teeri TT, Cottaz S, Planas A, Driguez H, Brumer H (2008) Mechanism-based labeling defines the free energy change for formation of the covalent glycosyl-enzyme intermediate in a xyloglucan endo-transglycosylase. J Biol Chem 283:21864–21872
Posé D, Castanedo I, Borsani O, Nieto B, Rosado A, Taconnat L, Ferrer A, Dolan L, Valpuesta V, Botella MA (2009) Identification of the Arabidopsis dry2/sqe1‐5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species. Plant J 59:63–76
Ranjan A, Pandey N, Lakhwani D, Dubey NK, Pathre UV, Sawant SV (2012) Comparative transcriptomic analysis of roots of contrasting Gossypium herbaceum genotypes revealing adaptation to drought. BMC Genomics 13:680
Rasbery JM, Shan H, LeClair RJ, Norman M, Matsuda SP, Bartel B (2007) Arabidopsis thaliana squalene epoxidase 1 is essential for root and seed development. J Biol Chem 282:17002–17013
Rashotte AM, DeLong A, Muday GK (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 13:1683–1697
Read DJ, Bartlett EM (1972) The psychology of drought resistance in the soy-bean plant (Glycine max). I. The relationship between drought resistance and growth. J Appl Ecol 9:487–499
Rodrigues ML, Pacheco CMA, Chaves MM (1995) Soil-plant water relations, root distribution and biomass partitioning in Lupinus albus L. under drought conditions. J Exp Bot 46:947–956
Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L (2000) Simultaneous analysis of metabolites in potato tuber by gas chromatography–mass spectrometry. Plant J 23:131–142
Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Gene Dev 17:354–358
Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17. 7. Plant Cell Rep 27:329–334
Serraj R, Shelp BJ, Sinclair TR (1998) Accumulation of γ‐aminobutyric acid in nodulated soybean in response to drought stress. Physiol Plant 102:79–86
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
Sevanto S (2014) Phloem transport and drought. J Exp Bot. doi:10.1093/jxb/ert467
Singh R, Pandey N, Naskar J, Shirke PA (2015) Physiological performance and differential expression profiling of genes associated with drought tolerance in contrasting varieties of two Gossypium species. Protoplasma 252:423–438
Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Youngs H (2004) Toward a systems approach to understanding plant cell walls. Science 306:2206–2211
Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M (2004) ydk1‐D, an auxin‐responsive GH3 mutant that is involved in hypocotyl and root elongation. Plant J 37:471–483
Taramino G, Sauer M, Stauffer JL, Multani D, Niu X, Sakai H, Hochholdinger F (2007) The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post‐embryonic shoot‐borne root initiation. Plant J 50:649–659
Tyree MT, Patiiio S, Bennink J, Alexander J (1995) Dynamic measurements of root hydraulic conductance using a high-pressure flowmeter in the laboratory and field. J Exp Bot 46:83–94
Acknowledgments
This work was supported by Council of Scientific and Industrial Research (CSIR), New Delhi, India (Grant No. OLP 085). A Senior Research Fellowship provided to RS and NP by Council of Scientific and Industrial Research (CSIR), New Delhi, India, is gratefully acknowledged.
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The authors wish to state that we have no conflict of interest.
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Handling Editor: Néstor Carrillo
Pramod A. Shirke holds PhD, CSIR—National Botanical Research Institute.
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Singh, R., Pandey, N., Kumar, A. et al. Physiological performance and differential expression profiling of genes associated with drought tolerance in root tissue of four contrasting varieties of two Gossypium species. Protoplasma 253, 163–174 (2016). https://doi.org/10.1007/s00709-015-0800-y
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DOI: https://doi.org/10.1007/s00709-015-0800-y