Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature

Xiangnan Li A B , Jian Cai A , Fulai Liu B C , Tingbo Dai A , Weixing Cao A and Dong Jiang A C

A National Engineering and Technology Center for Information Agriculture Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China.

B University of Copenhagen, Faculty of Science, Department of Plant and Environmental Sciences, Højbakkegaard Allé 13, DK-2630 Taastrup, Denmark.

C Corresponding authors. Emails: jiangd@njau.edu.cn; fl@life.ku.dk

Functional Plant Biology 41(7) 690-703 http://dx.doi.org/10.1071/FP13306
Submitted: 21 October 2013  Accepted: 20 January 2014   Published: 24 February 2014

Abstract

Spring low temperature events affect winter wheat (Triticum aestivum L.) during late vegetative or reproductive development, exposing plants to a subzero low temperature stress when winter hardening is lost. The increased climatic variability results in wheat being exposed to more frequent adverse impacts of combined low temperature and water stress, including drought and waterlogging. The responses of potted wheat plants cultivated in climatic chambers to these environmental perturbations were investigated at physiological, proteomic and transcriptional levels. At the physiological level, the depressed carbon (C) assimilation induced by the combined stresses was due mainly to stomatal closure and damage of photosynthetic electron transport. Biochemically, the adaptive effects of early moderate drought or waterlogging stress were associated with the activation of antioxidant enzyme system in chloroplasts and mitochondria of leaf under low temperature. Further proteomic analysis revealed that the oxidative stress defence, C metabolism and photosynthesis related proteins were modulated by the combined low temperature and water stress. Collectively, the results indicate that impairment of photosynthesis and C metabolism was responsible for the grain yield loss in winter wheat under low temperature in combination with severe drought or waterlogging stress. In addition, prior mild drought or waterlogging contributed to the homeostasis of oxidative metabolism and relatively better photosynthesis, and hence to less grain yield loss under later spring low temperature stress.

Additional keywords: low temperature, proteome, Triticum aestivum.


References

Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1–15.
Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta vulgaris.CrossRef | 1:CAS:528:DyaH1MXhtFaqtg%3D%3D&md5=994802752a64f327871eb14f54acacefCAS | 16654194PubMed | open url image1

Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Biology 50, 601–639.

Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391–396.
Production and scavenging of reactive oxygen species in chloroplasts and their functions.CrossRef | 1:CAS:528:DC%2BD28Xmt1aksbY%3D&md5=324c97753d7746c309fa21fbb5c58a3bCAS | 16760493PubMed | open url image1

Baek K-H, Skinner DZ (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines. Plant Science 165, 1221–1227.
Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines.CrossRef | 1:CAS:528:DC%2BD3sXos1KntLg%3D&md5=18d2f3f32eb8306f830c4b035a473213CAS | open url image1

Bazargani MM, Sarhadi E, Bushehri AA, Matros A, Mock HP, Naghavi MR, Hajihoseini V, Mardi M, Hajirezaei MR, Moradi F, Ehdaie B, Salekdeh GH (2011) A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. Journal of Proteomics 74, 1959–1973.
A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat.CrossRef | 1:CAS:528:DC%2BC3MXhtV2nur%2FL&md5=0dce4369b78a99076d33bacd60db4408CAS | 21621021PubMed | open url image1

Biemelt S, Keetman U, Albrecht G (1998) Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings. Plant Physiology 116, 651–658.
Re-aeration following hypoxia or anoxia leads to activation of the antioxidative defense system in roots of wheat seedlings.CrossRef | 1:CAS:528:DyaK1cXht1aisrw%3D&md5=33b7d31bf867357ae7fc990df6e54be4CAS | 9490765PubMed | open url image1

Biswas D, Jiang G (2011) Differential drought-induced modulation of ozone tolerance in winter wheat species. Journal of Experimental Botany 62, 4153–4162.
Differential drought-induced modulation of ozone tolerance in winter wheat species.CrossRef | 1:CAS:528:DC%2BC3MXhtVeit7nJ&md5=c287d0f49d69cf56a5a38f8e0afaf5efCAS | 21527624PubMed | open url image1

Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179–194.
Antioxidants, oxidative damage and oxygen deprivation stress: a review.CrossRef | 1:CAS:528:DC%2BD3sXitVCksbw%3D&md5=5c0fed6db8b8a8adde1e8a52695863fbCAS | 12509339PubMed | open url image1

Chen S, Zhou F, Yin C, Strasser RJ, Yang C, Qiang S (2011) Application of fast chlorophyll a fluorescence kinetics to probe action target of 3-acetyl-5-isopropyltetramic acid. Environmental and Experimental Botany 73, 31–41.
Application of fast chlorophyll a fluorescence kinetics to probe action target of 3-acetyl-5-isopropyltetramic acid.CrossRef | 1:CAS:528:DC%2BC3MXhtFGgtLfP&md5=38740f6793583a3f1721009ce518828eCAS | open url image1

Chen S, Yin C, Strasser RJ, Govindjee , Yang C, Qiang S (2012) Reactive oxygen species from chloroplasts contribute to 3-acetyl-5-isopropyltetramic acid-induced leaf necrosis of Arabidopsis thaliana. Plant Physiology and Biochemistry 52, 38–51.
Reactive oxygen species from chloroplasts contribute to 3-acetyl-5-isopropyltetramic acid-induced leaf necrosis of Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC38XhvVOku7c%3D&md5=0b99cd2825da055b8728323d6a75b522CAS | 22305066PubMed | open url image1

Dahal K, Kane K, Gadapati W, Webb E, Savitch LV, Singh J, Sharma P, Sarhan F, Longstaffe FJ, Grodzinski B, Huner NP (2012) The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus. Physiologia Plantarum 144, 169–188.
The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus.CrossRef | 1:CAS:528:DC%2BC38Xhs1Kjt7k%3D&md5=24a5112c0ba5a0dda65673353e925ac3CAS | 21883254PubMed | open url image1

Deng B, Du W, Liu C, Sun W, Tian S, Dong H (2012) Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids? Plant Growth Regulation 66, 37–47.
Antioxidant response to drought, cold and nutrient stress in two ploidy levels of tobacco plants: low resource requirement confers polytolerance in polyploids?CrossRef | 1:CAS:528:DC%2BC3MXhsFegsLrJ&md5=a536d73968ed9e226e7768b2ba15251aCAS | open url image1

Ding C, You J, Liu Z, Rehmani MIA, Wang S, Li G, Wang Q, Ding Y (2011) Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice. Plant Molecular Biology Reporter 29, 618–625.
Proteomic analysis of low nitrogen stress-responsive proteins in roots of rice.CrossRef | 1:CAS:528:DC%2BC3MXpsVCqs7g%3D&md5=18b4386cfb36d78881e07264866cea0cCAS | open url image1

Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33, 317–345.
Stomatal conductance and photosynthesis.CrossRef | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=3a73a520dccb5d008b17264757da14c1CAS | open url image1

Förster B, Osmond CB, Pogson BJ (2005) Improved survival of very high light and oxidative stress is conferred by spontaneous gain-of-function mutations in Chlamydomonas. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1709, 45–57.
Improved survival of very high light and oxidative stress is conferred by spontaneous gain-of-function mutations in Chlamydomonas.CrossRef | open url image1

Ge P, Ma C, Wang S, Gao L, Li X, Guo G, Ma W, Yan Y (2012) Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Analytical and Bioanalytical Chemistry 402, 1297–1313.
Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress.CrossRef | 1:CAS:528:DC%2BC3MXhsVGlsr7K&md5=3d0c8eda1d1ead767e506bee4aa1edb0CAS | 22080421PubMed | open url image1

Han Q, Kang G, Guo T (2013) Proteomic analysis of low temperature-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiology and Biochemistry 63, 236–244.
Proteomic analysis of low temperature-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.).CrossRef | 1:CAS:528:DC%2BC3sXhtlaktb0%3D&md5=533bc82d42ba64683166c8c36ea0bffdCAS | 23298682PubMed | open url image1

Hao J, Dong C, Zhang Z, Wang X, Shang Q (2012) Insights into salicylic acid responses in cucumber (Cucumis sativus L.) cotyledons based on a comparative proteomic analysis. Plant Science 187, 69–82.
Insights into salicylic acid responses in cucumber (Cucumis sativus L.) cotyledons based on a comparative proteomic analysis.CrossRef | 1:CAS:528:DC%2BC38XjsFKhur8%3D&md5=c4ca5ae5c311fc2e696fe831853f6e51CAS | 22404834PubMed | open url image1

Héroult A, Lin YS, Bourne A, Medlyn BE, Ellsworth DS (2013) Optimal stomatal conductance in relation to photosynthesis in climatically contrasting Eucalyptus species under drought. Plant, Cell & Environment 36, 262–274.
Optimal stomatal conductance in relation to photosynthesis in climatically contrasting Eucalyptus species under drought.CrossRef | open url image1

Hossain MA, Uddin SN (2011) Mechanisms of waterlogging tolerance in wheat: morphological and metabolic adaptations under hypoxia or anoxia. Australian Journal of Crop Science 5, 1094–1101.

Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiology 81, 802–806.
Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis.CrossRef | 1:CAS:528:DyaL28XltFWgu78%3D&md5=77feeb6beec4f9e098cfc477ef5e6c7eCAS | 16664906PubMed | open url image1

Iyer NJ, Tang Y, Mahalingam R (2013) Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula. Plant, Cell & Environment 36, 706–720.
Physiological, biochemical and molecular responses to a combination of drought and ozone in Medicago truncatula.CrossRef | 1:CAS:528:DC%2BC3sXhs1ais70%3D&md5=1bfdd59cbe52dc4444a0fa752f68c2c7CAS | open url image1

Jedmowski C, Ashoub A, Brüggemann W (2013) Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fluorescence transient analysis. Acta Physiologiae Plantarum 35, 345–354.
Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fluorescence transient analysis.CrossRef | open url image1

Jimenez A, Hernandez JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiology 114, 275–284.

Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant, Cell & Environment
Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept.CrossRef | open url image1

Kong FJ, Oyanagi A, Komatsu S (2010) Cell wall proteome of wheat roots under flooding stress using gel-based and LC MS/MS-based proteomics approaches. Biochimica et Biophysica Acta 1804, 124–136.
Cell wall proteome of wheat roots under flooding stress using gel-based and LC MS/MS-based proteomics approaches.CrossRef | 1:CAS:528:DC%2BD1MXhsVGru7rE&md5=97ae2f89c61117c4ab596961b27c0412CAS | 19786127PubMed | open url image1

Kreyling J, Wiesenberg GLB, Thiel D, Wohlfart C, Huber G, Walter J, Jentsch A, Konnert M, Beierkuhnlein C (2012) Cold hardiness of Pinus nigra Arnold as influenced by geographic origin, warming, and extreme summer drought. Environmental and Experimental Botany 78, 99–108.
Cold hardiness of Pinus nigra Arnold as influenced by geographic origin, warming, and extreme summer drought.CrossRef | open url image1

Li C, Jiang D, Wollenweber B, Li Y, Dai T, Cao W (2011) Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat. Plant Science 180, 672–678.
Waterlogging pretreatment during vegetative growth improves tolerance to waterlogging after anthesis in wheat.CrossRef | 1:CAS:528:DC%2BC3MXjtFGksrk%3D&md5=e7071249e0b064f2f44c55e72b268b4cCAS | 21421417PubMed | open url image1

Li H, Cai J, Liu F, Jiang D, Dai T, Cao W (2012) Generation and scavenging of reactive oxygen species in wheat flag leaves under combined shading and waterlogging stress. Functional Plant Biology 39, 71–81.
Generation and scavenging of reactive oxygen species in wheat flag leaves under combined shading and waterlogging stress.CrossRef | open url image1

Li X, Jiang H, Liu F, Cai J, Dai T, Cao W, Jiang D (2013) Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin. Plant Growth Regulation 71, 31–40.
Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin.CrossRef | 1:CAS:528:DC%2BC3sXht12is7jE&md5=305780ce5181eefb7c5f63c5e83bbdd1CAS | open url image1

Lidon FC, Loureiro AS, Vieira DE, Bilho EA, Nobre P, Costa R (2001) Photoinhibition in chilling stressed wheat and maize. Photosynthetica 39, 161–166.
Photoinhibition in chilling stressed wheat and maize.CrossRef | 1:CAS:528:DC%2BD3MXoslSrsb8%3D&md5=9c7485d0fc80817c32feebc7af60363dCAS | open url image1

Liu Y, Qi M, Li T (2012) Photosynthesis, photoinhibition, and antioxidant system in tomato leaves stressed by low night temperature and their subsequent recovery. Plant Science 196, 8–17.
Photosynthesis, photoinhibition, and antioxidant system in tomato leaves stressed by low night temperature and their subsequent recovery.CrossRef | 1:CAS:528:DC%2BC38XhsVamtbbK&md5=f365f4a8006a4f0e3d14e943f1213f34CAS | 23017895PubMed | open url image1

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔ C method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔ C method.CrossRef | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=bd84bb918d7f9eebed3fb6a0ab2babdbCAS | 11846609PubMed | open url image1

Mehler AH (1951) Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents. Archives of Biochemistry and Biophysics 33, 65–77.
Studies on reactions of illuminated chloroplasts: I. Mechanism of the reduction of oxygen and other hill reagents.CrossRef | 1:CAS:528:DyaG38XovFGg&md5=50086fa3ec0f7e8d24ac26c891c89315CAS | 14857775PubMed | open url image1

Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15–19.
Abiotic stress, the field environment and stress combination.CrossRef | 1:CAS:528:DC%2BD28XjvVKjsw%3D%3D&md5=5f2c3c3a8af878c57a41972a12256923CAS | 16359910PubMed | open url image1

Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiology 161, 5–19.
The impact of global change factors on redox signaling underpinning stress tolerance.CrossRef | 23151347PubMed | open url image1

Neumann PM (2008) Coping mechanisms for crop plants in drought-prone environments. Annals of Botany 101, 901–907.
Coping mechanisms for crop plants in drought-prone environments.CrossRef | 1:CAS:528:DC%2BD1cXntVaiurg%3D&md5=3b71345397b839782c532aa847712b38CAS | 18252764PubMed | open url image1

Nilsen ET, Orcutt DM (1996) ‘Physiology of plants under stress-abiotic factors.’ (John Wiley & Sons, New York)

Pang J, Zhou M, Mendham N, Shabala S (2004) Growth and physiological responses of six barley genotypes to waterlogging and subsequent recovery. Crop and Pasture Science 55, 895–906.
Growth and physiological responses of six barley genotypes to waterlogging and subsequent recovery.CrossRef | open url image1

Parry MAJ, John Andralojc P, Scales J, Salvucci M, Elizabete Carmo-Silva A, Hernan Alonso M, Whitney S (2013) Rubisco activity and regulation as targets for crop improvement. Journal of Experimental Botany 64, 717–730.
Rubisco activity and regulation as targets for crop improvement.CrossRef | 1:CAS:528:DC%2BC3sXhsFChur8%3D&md5=7c3ed492f6b174e953199f407f8ad67cCAS | open url image1

Pérez P, Morcuende R, Martín del Molino I, Martínez-Carrasco R (2005) Diurnal changes of Rubisco in response to elevated CO2, temperature and nitrogen in wheat grown under temperature gradient tunnels. Environmental and Experimental Botany 53, 13–27.
Diurnal changes of Rubisco in response to elevated CO2, temperature and nitrogen in wheat grown under temperature gradient tunnels.CrossRef | open url image1

Pérez P, Alonso A, Zita G, Morcuende R, Martínez-Carrasco R (2011) Down-regulation of Rubisco activity under combined increases of CO2 and temperature minimized by changes in Rubisco kcat in wheat. Plant Growth Regulation 65, 439–447.
Down-regulation of Rubisco activity under combined increases of CO2 and temperature minimized by changes in Rubisco kcat in wheat.CrossRef | open url image1

Piao S, Ciais P, Huang Y, Shen Z, Peng S, Li J, Zhou L, Liu H, Ma Y, Ding Y, Friedlingstein P, Liu C, Tan K, Yu Y, Zhang T, Fang J (2010) The impacts of climate change on water resources and agriculture in China. Nature 467, 43–51.
The impacts of climate change on water resources and agriculture in China.CrossRef | 1:CAS:528:DC%2BC3cXhtFSmsbzL&md5=948ddc091d47967f3e2d383bbc09e078CAS | 20811450PubMed | open url image1

Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C (2006) Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes. Plant, Cell & Environment 29, 2143–2152.
Drought stress response in wheat: physiological and molecular analysis of resistant and sensitive genotypes.CrossRef | 1:CAS:528:DC%2BD2sXhtVajtA%3D%3D&md5=092e17043f6065e4ddf05c4591ee1b1cCAS | open url image1

Rödiger A, Baudisch B, Bernd Klösgen R (2010) Simultaneous isolation of intact mitochondria and chloroplasts from a single pulping of plant tissue. Journal of Plant Physiology 167, 620–624.
Simultaneous isolation of intact mitochondria and chloroplasts from a single pulping of plant tissue.CrossRef | 20045215PubMed | open url image1

Ruelland E, Vaultier M-N, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. In ‘Advances in botanical research’. (Eds K Jean-Claude, D Michel) pp. 35–150. (Academic Press: New York)

Selote DS, Khanna-Chopra R (2006) Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings. Physiologia Plantarum 127, 494–506.
Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings.CrossRef | 1:CAS:528:DC%2BD28XosVKgsrc%3D&md5=ddf69cbe4f39c9d28e3bd0fdc97ca4faCAS | open url image1

Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
Fitting photosynthetic carbon dioxide response curves for C3 leaves.CrossRef | 1:CAS:528:DC%2BD2sXhtVeiur3F&md5=a98955521cb2fe2211000f28ffa89a52CAS | open url image1

Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annual Review of Biochemistry 75, 403–433.
Cold-adapted enzymes.CrossRef | 1:CAS:528:DC%2BD28XosVKhs7s%3D&md5=af2159c7fb024caf42f5cb8410d92f64CAS | 16756497PubMed | open url image1

Strasser RJ (1992) The F o and the OJIP fluorescence rise in higher plants and algae. In ‘Regulation of chloroplast biogenesis’. pp. 423–426. (Springer: Berlin)

Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing Photosynthesis: Mechanisms, Regulation and Adaptation 445–483.

Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. Chlorophyll a Fluorescence 321–362.
Analysis of the chlorophyll a fluorescence transient.CrossRef | 1:CAS:528:DC%2BD28XhtlagtL7K&md5=ff46eeaf695bea9d1e795f2811076ecdCAS | open url image1

Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16, 53–60.
Photoprotection in plants: a new light on photosystem II damage.CrossRef | 1:CAS:528:DC%2BC3MXjvFOgtw%3D%3D&md5=e86a07a0f00f7464ff6935885c141a60CAS | 21050798PubMed | open url image1

Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D (2008) Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica 46, 21–27.
Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging.CrossRef | 1:CAS:528:DC%2BD1cXjtlWgtbw%3D&md5=373f72aabe033071a525e52a1effa4b5CAS | open url image1

Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). Journal of Proteomics 71, 391–411.
Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP).CrossRef | 1:CAS:528:DC%2BD1cXhtFektr7K&md5=f23e1ffd68faeec72f1a0ccbdbd81513CAS | 18718564PubMed | open url image1

Walter J, Jentsch A, Beierkuhnlein C, Kreyling J (2012) Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. Environmental and Experimental Botany 94, 3–8.
Ecological stress memory and cross stress tolerance in plants in the face of climate extremes.CrossRef | open url image1

Wang Y, Lin A, Loake GJ, Chu C (2013) H2O2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species. Journal of Integrative Plant Biology 55, 202–208.
H2O2-induced leaf cell death and the crosstalk of reactive nitric/oxygen species.CrossRef | 1:CAS:528:DC%2BC3sXntVags7k%3D&md5=282a04aa05578e7025fe3a96a286c461CAS | 23331502PubMed | open url image1

Weldearegay D, Yan F, Jiang D, Liu F (2012) Independent and combined effects of soil warming and drought stress during anthesis on seed set and grain yield in two spring wheat varieties. Journal Agronomy & Crop Science 198, 245–253.
Independent and combined effects of soil warming and drought stress during anthesis on seed set and grain yield in two spring wheat varieties.CrossRef | open url image1

Xu J, Li Y, Sun J, Du L, Zhang Y, Yu Q, Liu X (2013) Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance. Plant Biology 15, 292–303.
Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance.CrossRef | 1:CAS:528:DC%2BC3sXjvVOlt7s%3D&md5=9a711b0415262338f49f69aa56b651a2CAS | 22963252PubMed | open url image1

Yang S-H, Wang L-J, Li S-H (2007) Ultraviolet-B irradiation-induced low temperature tolerance in relation to antioxidant system in winter wheat (Triticum aestivum L.) leaves. Environmental and Experimental Botany 60, 300–307.
Ultraviolet-B irradiation-induced low temperature tolerance in relation to antioxidant system in winter wheat (Triticum aestivum L.) leaves.CrossRef | 1:CAS:528:DC%2BD2sXntFyht7c%3D&md5=d678e423a560dcd81e38fdaa0732307aCAS | open url image1

Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. Journal of Plant Physiology 167, 959–966.
Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves.CrossRef | 1:CAS:528:DC%2BC3cXpsVClsbw%3D&md5=4a3a72159715f97e898109157c34c90eCAS | 20417985PubMed | open url image1

Zhang X, Jiang D, Zheng C, Dai T, Cao W (2011) Post-anthesis salt and combination of salt and waterlogging affect distributions of sugars, amino acids, Na+ and K+ in wheat. Journal Agronomy & Crop Science 197, 31–39.
Post-anthesis salt and combination of salt and waterlogging affect distributions of sugars, amino acids, Na+ and K+ in wheat.CrossRef | 1:CAS:528:DC%2BC3MXhvV2ktLo%3D&md5=a7c41a267baa6a0581929aeeab825461CAS | open url image1

Zhang X, Cai J, Wollenweber B, Liu F, Dai T, Cao W, Jiang D (2013) Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat. Journal of Cereal Science 57, 134–140.
Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat.CrossRef | 1:CAS:528:DC%2BC38XhvVWisrnE&md5=8f4a1448b61b5ae51422cbebf3c89193CAS | open url image1

Zheng C, Jiang D, Liu F, Dai T, Jing Q, Cao W (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Science 176, 575–582.
Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat.CrossRef | 1:CAS:528:DC%2BD1MXisFGkuro%3D&md5=ae365764e660cac204b25aea800bb757CAS | open url image1

Zhong X, Mei X, Li Y, Yoshida H, Zhao P, Wang X, Han L, Hu X, Huang S, Huang J, Sun Z (2008) Changes in frost resistance of wheat young ears with development during jointing stage. Journal Agronomy & Crop Science 194, 343–349.
Changes in frost resistance of wheat young ears with development during jointing stage.CrossRef | open url image1



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