Understanding the molecular events underpinning cultivar differences in the physiological performance and heat tolerance of cotton (Gossypium hirsutum)
Nicola S. Cottee A D , Iain W. Wilson B , Daniel K. Y. Tan C and Michael P. Bange A
+ Author Affiliations
- Author Affiliations
A CSIRO Plant Industry, Locked Bag 59, Narrabri, NSW 2390, Australia.
B CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.
C Faculty of Agriculture and Environment, The University of Sydney, Sydney, NSW 2006, Australia.
D Corresponding author. Email: nicola.cottee@csiro.au
Functional Plant Biology 41(1) 56-67 https://doi.org/10.1071/FP13140
Submitted: 15 May 2013 Accepted: 12 July 2013 Published: 9 August 2013
Abstract
Diurnal or prolonged exposure to air temperatures above the thermal optimum for a plant can impair physiological performance and reduce crop yields. This study investigated the molecular response to heat stress of two high-yielding cotton (Gossypium hirsutum L.) cultivars with contrasting heat tolerance. Using global gene profiling, 575 of 21854 genes assayed were affected by heat stress, ~60% of which were induced. Genes encoding heat shock proteins, transcription factors and protein cleavage enzymes were induced, whereas genes encoding proteins associated with electron flow, photosynthesis, glycolysis, cell wall synthesis and secondary metabolism were generally repressed under heat stress. Cultivar differences for the expression profiles of a subset of heat-responsive genes analysed using quantitative PCR over a 7-h heat stress period were associated with expression level changes rather than the presence or absence of transcripts. Expression differences reflected previously determined differences for yield, photosynthesis, electron transport rate, quenching, membrane integrity and enzyme viability under growth cabinet and field-generated heat stress, and may explain cultivar differences in leaf-level heat tolerance. This study provides a platform for understanding the molecular changes associated with the physiological performance and heat tolerance of cotton cultivars that may aid breeding for improved performance in warm and hot field environments.
Additional keywords: electron transport, heat stress, membrane integrity, microarray, Rubisco, quantitative real-time polymerase chain reaction.
References
Bernardo R (2002) ‘Breeding for quantitative traits in plants.’ (Stemma Press: Woodbury, MN)Bibi A, Oosterhuis DM, Gonias ED (2008) Photosynthesis, quantum yield of photosystem II and membrane leakage as affected by high temperatures in cotton genotypes. Journal of Cotton Science 12, 150–159.
Boscaiu M, Donat P, Llinares J, Vicente O (2012) Stress-tolerant wild plants: a source of knowledge and biotechnological tools for the genetic improvement of stress tolerance in crop plants. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 40, 323–327.
Burke JJ, Mahan JR, Hatfield JL (1988) Crop-specific thermal kinetic windows in relation to wheat and cotton biomass production. Agronomy Journal 80, 553–556.
| Crop-specific thermal kinetic windows in relation to wheat and cotton biomass production.Crossref | GoogleScholarGoogle Scholar |
Busch W, Wunderlick M, Schoffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. The Plant Journal 41, 1–14.
| Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWjsLo%3D&md5=ad6968459dd2eb121e3b6ceb0860e92bCAS | 15610345PubMed |
Cadman CSC, Toorop PE, Hilhorst HWM, Finch-Savage WE (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. The Plant Journal 46, 805–822.
| Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmvVWqur0%3D&md5=2be2e6edd1326104138decc86529a206CAS |
Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiology 143, 251–262.
| A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1OntQ%3D%3D&md5=a02652fe51d621c71157cc715a0dfcfdCAS | 17085506PubMed |
Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). Plant & Cell Physiology 51, 21–37.
| Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntlKqsw%3D%3D&md5=03f171007710e8674274df38a37750ddCAS |
Constable GA (2000) Variety: ‘Sicot 53’. Application number: 1999/264. Plant Varieties Journal 13, 47–48.
Cottee NS, Tan DKY, Bange MP, Cothren JT, Campbell LCC (2010) Multi-level determination of heat tolerance in cotton (Gossypium hirsutum L.) under field conditions. Crop Science 50, 2553–2564.
| Multi-level determination of heat tolerance in cotton (Gossypium hirsutum L.) under field conditions.Crossref | GoogleScholarGoogle Scholar |
Cottee NS, Bange MP, Wilson IW, Tan DKY (2012) Developing controlled environment screening for high-temperature tolerance in cotton that accurately reflects performance in the field. Functional Plant Biology 39, 670–678.
| Developing controlled environment screening for high-temperature tolerance in cotton that accurately reflects performance in the field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1Smu7bO&md5=c3969c4bc0aff34bc5b72ec9bef80e5dCAS |
Dash S, Van Hemert J, Hong L, Wise R, Dickerson J (2012) PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Research 40, D1194–D1201.
| PLEXdb: gene expression resources for plants and plant pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs12hurjJ&md5=27276369d76a4b58fcd4379b4bdb3177CAS | 22084198PubMed |
de Ronde JA, van der Mescht A (1997) 2,3,5-Triphenyltetrazolium chloride reduction as a measure of drought tolerance and heat tolerance in cotton. South African Journal of Science 93, 431–433.
de Ronde JA, van der Mescht A, Cress WA (1993) Heat-shock protein synthesis in cotton is cultivar dependent. South African Journal of Plant and Soil 10, 95–97.
DeRidder BP, Salvucci ME (2007) Modulation of Rubisco activase gene expression during heat stress in cotton (Gossypium hirsutum L.) involves post-transcriptional mechanisms. Plant Science 172, 246–254.
| Modulation of Rubisco activase gene expression during heat stress in cotton (Gossypium hirsutum L.) involves post-transcriptional mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFKgtA%3D%3D&md5=22be3e98b9a7d0f61ce3787d6506a836CAS |
Dev Sharma A, Kumar S, Singh P (2006) Expression analysis of stress-modulated transcript in drought tolerant and susceptible cultivars of sorghum (Sorghum bicolor). Journal of Plant Physiology 163, 570–576.
| Expression analysis of stress-modulated transcript in drought tolerant and susceptible cultivars of sorghum (Sorghum bicolor).Crossref | GoogleScholarGoogle Scholar | 16473662PubMed |
Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. The Plant Cell 12, 393–404.
Haußühl K, Andersson B, Adamska I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. The EMBO Journal 20, 713–722.
| A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II.Crossref | GoogleScholarGoogle Scholar | 11179216PubMed |
Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiology 116, 439–444.
| The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslGiug%3D%3D&md5=578f4ea177da54632db0a05ebfe2d72cCAS | 9449851PubMed |
Hewezi T, Léger M, Gentzbittel L (2008) A comprehensive analysis of the combined effects of high light and high temperature stresses on gene expression in sunflower. Annals of Botany 102, 127–140.
| A comprehensive analysis of the combined effects of high light and high temperature stresses on gene expression in sunflower.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Kgsro%3D&md5=eaac5ef647fb5072057af9c324e337adCAS | 18477560PubMed |
Hong S-W, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proceedings of the National Academy of Sciences of the United States of America 97, 4392–4397.
| Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSnsLw%3D&md5=ac16b994078825cabd5cd52f4f04e48cCAS | 10760305PubMed |
Howarth CJ (1991) Molecular response of plants to an increased incidence of heat shock. Plant, Cell & Environment 14, 831–841.
| Molecular response of plants to an increased incidence of heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xht1Crs7s%3D&md5=1c94a1be51d0a5fa4607808d92d24b88CAS |
Humphreys MO, Humphreys MW (2005) Breeding for stress resistance: general principles. In ‘Abiotic stresses, plant resistance through breeding and molecular approaches’. (Eds M Ashraf, PJC Harris.) pp. 19–46. (The Haworth Press: Binghamton, NY)
Kant P, Gordon M, Kant S, Zolla G, Davydov O, Heimer Y, Chalifa-Caspi V, Shaked R, Barak S (2008) Function-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant, Cell & Environment 31, 697–714.
| Function-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVOmtLk%3D&md5=0400244edf858f8600aa4b276d0181abCAS |
Kimura A, Eaton-Rye JJ, Morita EH, Nishiyama Y, Hayashi H (2002) Protection of the oxygen-evolving machinery by the extrinsic proteins of photosystem II is essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant & Cell Physiology 43, 932–938.
| Protection of the oxygen-evolving machinery by the extrinsic proteins of photosystem II is essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsFOkurk%3D&md5=1cb812cda2969fe00df06ea5d27f2418CAS |
Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiology 146, 748–761.
| Core genome responses involved in acclimation to high temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFCmtbs%3D&md5=d6e10ac472327d468830fc5554dc6da1CAS | 18055584PubMed |
Leone A, Perrotta C, Maresca B (2003) Plant tolerance to heat stress: current strategies and new emergent insights. In ‘Abiotic stresses in plants’. (Eds L Sanita di Toppi, B Pawlik-Skowronska) pp. 1–22. (Kluwer Academic Publishers: Dordrecht)
Lim CJ, Yang KA, Hong JK, Choi AS, Yun DJ, Hong JC, Chung WS, Lee SY, Cho MJ, Lim CO (2006) Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells. Journal of Plant Research 119, 373–383.
| Gene expression profiles during heat acclimation in Arabidopsis thaliana suspension-culture cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt1agtLo%3D&md5=92660b801e7ab93fd93958cda5f5ecd7CAS | 16807682PubMed |
Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. The Plant Journal 20, 89–99.
| Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnsVGru7c%3D&md5=44af2eaa197abfa2ca33bdb44ba96908CAS | 10571868PubMed |
Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf K-D (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes & Development 16, 1555–1567.
| In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVGmtb4%3D&md5=277f2872c70e939bce122adfcf15ebf7CAS |
Nieto-Sotelo J, Martinez LM, Ponce G, Cassab GI, Alagon A, Meeley RB, Ribaut J-M, Yang R (2002) Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth. The Plant Cell 14, 1621–1633.
| Maize HSP101 plays important roles in both induced and basal thermotolerance and primary root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvV2rsbc%3D&md5=1cc93eee1cf64087cb0a0342a42999fcCAS | 12119379PubMed |
Ogawa T, Pan L, Kawai-Yamada M, Yu L-H, Yamamura S, Koyama T, Kitajima S, Ohme-Takagi M, Sato F, Uchimiya H (2005) Functional analysis of Arabidopsis ethylene-responsive element binding protein conferring resistance to Bax and abiotic stress-induced plant cell death. Plant Physiology 138, 1436–1445.
| Functional analysis of Arabidopsis ethylene-responsive element binding protein conferring resistance to Bax and abiotic stress-induced plant cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2lu7c%3D&md5=221fb5d07c89aaf36533c3d80b1da56fCAS | 15980186PubMed |
Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. Journal of Experimental Botany 58, 3373–3383.
| High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Kmt7zL&md5=0ec2c32e7506d78b048833254fbf1143CAS | 17890230PubMed |
Padmalatha KV, Dhandapani G, Kanakachari M, Kumar S, Dass A, Patil DP, Rajamani V, Kumar K, Pathak R, Rawat B, Leelavathi S, Reddy PS, Jain N, Powar KN, Hiremath V, Katageri IS, Reddy MK, Solanke AU, Reddy VS, Kumar PA (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Molecular Biology 78, 223–246.
| Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVSjtw%3D%3D&md5=b9d4c10f9357c105313b8498caad077dCAS | 22143977PubMed |
Panchuk II, Volkov RA, Schoffl F (2002) Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiology 129, 838–853.
| Heat stress- and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2jtL4%3D&md5=eff7adf161860a7a35eb5c0c6b93a173CAS | 12068123PubMed |
Park W, Scheffler BE, Bauer PJ, Campbell BT (2012) Genome-wide identification of differentially expressed genes under water deficit stress in upland cotton (Gossypium hirsutum L.). BMC Plant Biology 12, 90
| Genome-wide identification of differentially expressed genes under water deficit stress in upland cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslals7vO&md5=76250fbc2d8c96a57dd3282539caa2caCAS | 22703539PubMed |
Payton P, Kottapalli KR, Kebede H, Mahan JR, Wright RJ, Allen RD (2011) Examining the drought stress transcriptome in cotton leaf and root tissue. Biotechnology Letters 33, 821–828.
| Examining the drought stress transcriptome in cotton leaf and root tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFemtrk%3D&md5=338aa4ecba89d591faf574aeca15035bCAS | 21188619PubMed |
Pettigrew WT, Turley RB (1998) Variation in photosynthetic components among photosynthetically diverse cotton genotypes. Photosynthesis Research 56, 15–25.
| Variation in photosynthetic components among photosynthetically diverse cotton genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltlKrtL4%3D&md5=7edb3d56c462b0c6e79fbee089c497b3CAS |
Rahman H, Bibi A, Latif M (2005) Okra-leaf accessions of the upland cotton (Gossypium hirsutum L.): genetic variability in agronomic and fibre traits. Journal of Applied Genetics 46, 149–155.
Reddy VR, Baker DN, Hodges HF (1991) Temperature effects on cotton canopy growth, photosynthesis and respiration. Agronomy Journal 83, 699–704.
| Temperature effects on cotton canopy growth, photosynthesis and respiration.Crossref | GoogleScholarGoogle Scholar |
Reid PE (2004) Variety: ‘Sicala 45’. Application number: 2003/038. Plant Varieties Journal 17, 174–176.
Reid PE, Thomson NJ, Lawrence PK, Luckett DJ, McIntyre GT, Williams ER (1989) Regional evaluation of cotton cultivars in eastern Australia, 1974–85. Australian Journal of Experimental Agriculture 29, 679–689.
| Regional evaluation of cotton cultivars in eastern Australia, 1974–85.Crossref | GoogleScholarGoogle Scholar |
Rensink WA, Iobst S, Hart A, Stegalkina S, Liu J, Buell CR (2005) Gene expression profiling of potato responses to cold, heat, and salt stress. Functional & Integrative Genomics 5, 201–207.
| Gene expression profiling of potato responses to cold, heat, and salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVajsLjE&md5=cc4973da0efd732a663a8ecd3f31dc34CAS |
Rizhsky L, Liang HJ, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology 130, 1143–1151.
| The combined effect of drought stress and heat shock on gene expression in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOnu7c%3D&md5=0a61e1ddaeb777cd160c58a2664478a6CAS | 12427981PubMed |
Rizhsky L, Liang HJ, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683–1696.
| When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKmsbs%3D&md5=d9e844edb88c1fffa807eff545cac654CAS | 15047901PubMed |
Rodriguez-Uribe L, Zhang J (2009) ‘GSE18253: Gene expression profiling in drought tolerant Acala 1517–99 cotton (Gossypium hirsutum L.) under reduced irrigation field conditions.’ Available at http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE18253 [Verified 26 July 2013].
Ryan PR, Liu Q, Sperling P, Dong B, Franke S, Delhaize E (2007) A higher plant Δ8 sphingolipid desaturase with a preference for (Z)-Isomer formation confers aluminum tolerance to yeast and plants. Plant Physiology 144, 1968–1977.
| A higher plant Δ8 sphingolipid desaturase with a preference for (Z)-Isomer formation confers aluminum tolerance to yeast and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVOgsLw%3D&md5=ce0921fecb672b7026c34610a94c8d26CAS | 17600137PubMed |
Sahi C, Agarwal M, Reddy M, Sopory S, Grover A (2003) Isolation and expression of salt stress-associated ESTs from contrasting rice cultivars using a PCR-based subtraction method. Theoretical and Applied Genetics 106, 620–628.
Salvucci ME (2008) Association of Rubisco activase with chaperionin-60β: a possible mechanism for protecting photosynthesis during heat stress. Journal of Experimental Botany 59, 1923–1933.
| Association of Rubisco activase with chaperionin-60β: a possible mechanism for protecting photosynthesis during heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtleltr8%3D&md5=b3f8f43c257b97ecd9befad67cfbf2d7CAS | 18353762PubMed |
Shavrukov Y (2013) Salt stress or salt shock: which genes are we studying? Journal of Experimental Botany 64, 119–127.
| Salt stress or salt shock: which genes are we studying?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2gsbnN&md5=48fc673eb705c2b6f4b32fb5f004ee22CAS | 23186621PubMed |
Smith AMO, Ratcliffe RG, Sweetlove LJ (2004) Activation and function of mitochondrial uncoupling protein in plants. The Journal of Biological Chemistry 279, 51944–51952.
| Activation and function of mitochondrial uncoupling protein in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCktbjI&md5=9af2e4a80073639c1d7cad5facddc0f8CAS |
Sotirios KA, Argyrokastritis A, Loukas M, Eliopoulos E, Tsakas S, Kaltsikes PJ (2006) Isolation and characterization of stress related heat shock protein calmodulin binding gene from cultivated cotton (Gossypium hirsutum L.). Euphytica 147, 343–351.
| Isolation and characterization of stress related heat shock protein calmodulin binding gene from cultivated cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvF2lsLc%3D&md5=c26285d6b24083ce968988daa7466cd1CAS |
Sullivan CY (1971) Mechanisms of heat and drought resistance in grain sorghum and methods of measurement. In ‘Sorghum in the seventies’. (Eds NGP Rao, LR House) pp. 247–284. (Oxford & IBH Publishing Co: New Delhi)
Taiz L, Zeiger E (2006) ‘Plant physiology.’ (Sinauer Associates: Sunderland, MA)
Tanaka K, Asami T, Yoshida S, Nakamurra Y, Matsuo T (2005) Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism. Plant Physiology 138, 1117–1125.
| Brassinosteroid homeostasis in Arabidopsis is ensured by feedback expressions of multiple genes involved in its metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVejsLc%3D&md5=1a8916e61d01e564cc540a75bf316d06CAS | 15908602PubMed |
Tardieu F, Hammer G (2012) Designing crops for new challenges. European Journal of Agronomy 42, 1–2.
| Designing crops for new challenges.Crossref | GoogleScholarGoogle Scholar |
Tian J, Belanger FC, Huang B (2009) Identification of heat stress-responsive genes in heat-adapted thermal Agrostis scabra by suppression subtractive hybridization. Journal of Plant Physiology 166, 588–601.
| Identification of heat stress-responsive genes in heat-adapted thermal Agrostis scabra by suppression subtractive hybridization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktlSgu7o%3D&md5=b9befff8dc7589ef0f58ca0960a18cd1CAS | 18950897PubMed |
ur Rahman H, Malik SA, Saleem M (2004) Heat tolerance of upland cotton during the fruiting stage evaluated using cellular membrane thermostability. Field Crops Research 85, 149–158.
| Heat tolerance of upland cotton during the fruiting stage evaluated using cellular membrane thermostability.Crossref | GoogleScholarGoogle Scholar |
Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible W, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses. Plant Physiology 138, 1195–1204.
| Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2ltbY%3D&md5=8fc370c813a4ca3a6efc0b69200126d7CAS | 16009995PubMed |
Voloudakis AE, Kosmas SA, Tsakas S, Eliopoulos E, Loukas M, Kosmidou K (2002) Expression of selected drought-related genes and physiological response of Greek cotton varieties. Functional Plant Biology 29, 1237–1245.
| Expression of selected drought-related genes and physiological response of Greek cotton varieties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xoslentr4%3D&md5=34a8919ad71cea5a5cb178d688ecd08dCAS |
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227, 957–967.
| Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsF2isLc%3D&md5=68cabc0dc5337317b44f7431a60f1031CAS | 18064488PubMed |
Zhang Y, Rouf Mian MA, Chekhovskiy K, So S, Kupfer D, Lai H, Roe BA (2005) Differential gene expression in Festuca under heat stress conditions. Journal of Experimental Botany 56, 897–907.
| Differential gene expression in Festuca under heat stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1Kntbc%3D&md5=d2a44a62559e6dace4e9d5311840d998CAS | 15710639PubMed |
