Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability (original) (raw)

• Bailey-Serres, J., Lee, S. C. & Brinton, E. Waterproofing crops: effective flooding survival strategies. Plant Physiol. 160, 1698–1709 (2012).
  CAS PubMed PubMed Central Google Scholar
• Boyer, J. S. et al. The U.S. drought of 2012 in perspective: a call to action. Global Food Secur. 2, 139–143 (2013).
  Google Scholar
• Hirabayashi, Y. et al. Global flood risk under climate change. Nature Clim. Chang. 3, 816–821 (2013).
  Google Scholar
• Pryor, S. C., Barthelmie, R. J. & Schoof, J. T. High-resolution projections of climate-related risks for the Midwestern USA. Clim. Res. 56, 61–79 (2013).
  Google Scholar
• Bita, C. E. & Gerats, T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front. Plant Sci. 4, 273 (2013).
  PubMed PubMed Central Google Scholar
• Gourdji, S. M., Sibley, A. M. & Lobell, D. B. Global crop exposure to critical high temperatures in the reproductive period: historical trends and future projections. Environ. Res. Lett. 8, 024041 (2013).
  Google Scholar
• Rosenzweig, C. et al. Assessing agricultural risks of climate change in the 21st century in a global gridded crop model intercomparison. Proc. Natl Acad. Sci. USA 111, 3268–3273 (2014).
  CAS PubMed Google Scholar
• Iizumi, T. et al. Prediction of seasonal climate-induced variations in global food production. Nature Clim. Chang. 3, 904–908 (2013).
  Google Scholar
• Intergovernmental Panel on Climate Change, 2014. Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) [online], (Cambridge University Press, 2014).
• Lobell, D. B. et al. Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science 344, 516–519 (2014).
  CAS PubMed Google Scholar
• Mansouri-Far, C., Modarres Sanavy, S. A. M. & Saberali, S. F. Maize yield response to deficit irrigation during low-sensitive growth stages and nitrogen rate under semi-arid climatic conditions. Agr. Water Manage. 97, 12–22 (2010).
  Google Scholar
• Takeda, S. & Matsuoka, M. Genetic approaches to crop improvement: responding to environmental and population changes. Nature Rev. Genet. 9, 444–457 (2008).
  CAS PubMed Google Scholar
• Gamuyao, R. et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488, 535–539 (2012). PSTOL1 , a gene that regulates crown root development and root biomass, is shown to provide tolerance to low-P soils in rice.
  CAS PubMed Google Scholar
• Xu, K. et al. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708 (2006). A rice gene found in a farmer's landrace is identified as an ERF that confers tolerance of prolonged submergence on O. sativa ssp. indica and O. sativa ssp. japonica varieties of rice.
  CAS PubMed Google Scholar
• Niroula, R. K. et al. _SUB1A_-dependent and -independent mechanisms are involved in the flooding tolerance of wild rice species. Plant J. 72, 282–293 (2012).
  CAS PubMed Google Scholar
• Singh, N. et al. Molecular marker survey and expression analyses of the rice submergence-tolerance gene SUB1A. Theor. Appl. Genet. 121, 1441–1453 (2010).
  CAS PubMed Google Scholar
• Fukao, T., Xu, K., Ronald, P. C. & Bailey-Serres, J. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18, 2021–2034 (2006). The mode of action of SUB1A is shown to involve the conservation of carbohydrate catabolism and the minimization of underwater elongation growth in rice.
  CAS PubMed PubMed Central Google Scholar
• Fukao, T. & Bailey-Serres, J. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc. Natl Acad. Sci. USA 105, 16814–16819 (2008).
  CAS PubMed PubMed Central Google Scholar
• Fukao, T., Yeung, E. & Bailey-Serres, J. The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice. Plant Physiol. 160, 1795–1807 (2012).
  CAS PubMed PubMed Central Google Scholar
• Fukao, T., Yeung, E. & Bailey-Serres, J. The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell 23, 412–427 (2011).
  CAS PubMed Google Scholar
• Septiningsih, E. M. et al. in Translational Genomics for Crop Breeding (eds Varshney, R. K. & Tuberosa, R.) 9–30 (Wiley, 2013).
  Google Scholar
• Dar, M. H., de Janvry, A., Emerick, K., Raitzer, D. & Sadoulet, E. Flood-tolerant rice reduces yield variability and raises expected yield, differentially benefitting socially disadvantaged groups. Sci. Rep. 3, 3315 (2013).
  PubMed PubMed Central Google Scholar
• Singh, S., Mackill, D. J. & Ismail, A. M. Responses of SUB1 rice introgression lines to submergence in the field: yield and grain quality. Field Crops Res. 113, 12–23 (2009).
  Google Scholar
• Hattori, Y. et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460, 1026–1030 (2009). One of three QTLs present in deepwater rice that are necessary and sufficient to promote rapid underwater elongation growth encodes two ERFs related to SUB1A.
  CAS PubMed Google Scholar
• Ayano, M. et al. Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice. Plant Cell Environ. 37, 2313–2324 (2014).
  CAS PubMed PubMed Central Google Scholar
• Gibbs, D. J. et al. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 479, 415–418 (2011).
  CAS PubMed PubMed Central Google Scholar
• Licausi, F. et al. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479, 419–422 (2011). References 26 and 27 show that the SUB1A-like ERFs of A. thaliana are targets of an oxygen-dependent branch of the N-end rule pathway.
  CAS PubMed Google Scholar
• van Veen, H. et al. Two Rumex species from contrasting hydrological niches regulate flooding tolerance through distinct mechanisms. Plant Cell 25, 4691–4707 (2013).
  CAS PubMed PubMed Central Google Scholar
• Malik, A. I., Islam, A. K. & Colmer, T. D. Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four _H. marinum_–wheat amphiploids. New Phytol. 190, 499–508 (2011).
  CAS PubMed Google Scholar
• Abiko, T. et al. Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant Cell Environ. 35, 1618–1630 (2012).
  CAS PubMed Google Scholar
• Mano, Y. & Omori, F. Flooding tolerance in interspecific introgression lines containing chromosome segments from teosinte (Zea nicaraguensis) in maize (Zea mays subsp. mays). Ann. Bot. 112, 1125–1139 (2013).
  CAS PubMed PubMed Central Google Scholar
• Weber, V. S. et al. Efficiency of managed-stress screening of elite maize hybrids under drought and low nitrogen for yield under rainfed conditions in southern Africa. Crop Sci. 52, 1011–1020 (2012).
  Google Scholar
• Hu, H. & Xiong, L. Genetic engineering and breeding of drought-resistant crops. Annu. Rev. Plant Biol. 65, 715–741 (2014).
  CAS PubMed Google Scholar
• Xu, J. et al. Identification of candidate genes for drought tolerance by whole-genome resequencing in maize. BMC Plant Biol. 14, 83 (2014).
  PubMed PubMed Central Google Scholar
• Sandhu, N. et al. Identification and mapping of stable QTL with main and epistasis effect on rice grain yield under upland drought stress. BMC Genet. 15, 63 (2014).
  PubMed PubMed Central Google Scholar
• Ravi, K. et al. Identification of several small main-effect QTLs and a large number of epistatic QTLs for drought tolerance related traits in groundnut (Arachis hypogaea L.). Theor. Appl. Genet. 122, 1119–1132 (2011).
  CAS PubMed Google Scholar
• Swamy, B. P. et al. Genetic, physiological, and gene expression analyses reveal that multiple QTL enhance yield of rice mega-variety IR64 under drought. PLoS ONE 8, e62795 (2013).
  PubMed Google Scholar
• Makumburage, G. B. et al. Genotype to phenotype maps: multiple input abiotic signals combine to produce growth effects via attenuating signaling interactions in maize. G3 (Bethesda) 3, 2195–2204 (2013).
  Google Scholar
• Tardieu, F. Any trait or trait-related allele can confer drought tolerance: just design the right drought scenario. J. Exp. Bot. 63, 25–31 (2012).
  CAS PubMed Google Scholar
• Semagn, K. et al. Meta-analyses of QTL for grain yield and anthesis silking interval in 18 maize populations evaluated under water-stressed and well-watered environments. BMC Genomics 14, 313 (2013).
  PubMed PubMed Central Google Scholar
• Uga, Y., Okuno, K. & Yano, M. Dro1, a major QTL involved in deep rooting of rice under upland field conditions. J. Exp. Bot. 62, 2485–2494 (2011).
  CAS PubMed Google Scholar
• Uga, Y. et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature Genet. 45, 1097–1102 (2013). A gene determining the downward growth of roots is identified and shown to contribute to avoidance of drought in rice.
  CAS PubMed Google Scholar
• Arai-Sanoh, Y. et al. Deep rooting conferred by DEEPER ROOTING 1, enhances rice yield in paddy fields. Sci. Rep. 4, 5563 (2014).
  CAS PubMed PubMed Central Google Scholar
• Burton, A. L. et al. QTL mapping and phenotypic variation for root architectural traits in maize (Zea mays L.). Theor. Appl. Genet. 127, 2293–2311 (2014).
  PubMed Google Scholar
• Placido, D. F. et al. Introgression of novel traits from a wild wheat relative improves drought adaptation in wheat. Plant Physiol. 161, 1806–1819 (2013).
  CAS PubMed PubMed Central Google Scholar
• Mace, E. S. et al. QTL for nodal root angle in sorghum (Sorghum bicolor L. Moench) co-locate with QTL for traits associated with drought adaptation. Theor. Appl. Genet. 124, 97–109 (2012).
  CAS PubMed Google Scholar
• Naz, A. A., Arifuzzaman, M., Muzammil, S., Pillen, K. & Leon, J. Wild barley introgression lines revealed novel QTL alleles for root and related shoot traits in the cultivated barley (Hordeum vulgare L.). BMC Genet. 15, 107 (2014).
  PubMed PubMed Central Google Scholar
• Varshney, R. K. et al. Fast-track introgression of “_QTL-hotspot_” for root traits and other drought tolerance traits in JG 11, an elite and leading variety of chickpea (Cicer arietinum L.). Plant Genome http://dx.doi.org/10.3835/plantgenome2013.07.0022 (2013).
• Kollist, H., Nuhkat, M. & Roelfsema, M. R. Closing gaps: linking elements that control stomatal movement. New Phytol. 203, 44–62 (2014).
  CAS PubMed Google Scholar
• Daszkowska-Golec, A. & Szarejko, I. Open or close the gate — stomata action under the control of phytohormones in drought stress conditions. Front. Plant Sci. 4, 138 (2013).
  PubMed PubMed Central Google Scholar
• Danquah, A., de Zelicourt, A., Colcombet, J. & Hirt, H. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol. Adv. 32, 40–52 (2014).
  CAS PubMed Google Scholar
• Ma, Y. et al. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064–1068 (2009). A receptor of ABA is identified and shown to regulate signal transduction through interaction with a protein phosphatase.
  CAS PubMed Google Scholar
• Park, S.-Y. et al. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071 (2009). An ABA-binding protein is identified through the use of a chemical agonist and genetic screening; the binding of the hormone to the receptor limits negative regulation of signalling.
  CAS PubMed PubMed Central Google Scholar
• Fujii, H. et al. In vitro reconstitution of an abscisic acid signalling pathway. Nature 462, 660–664 (2009).
  CAS PubMed PubMed Central Google Scholar
• Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R. & Abrams, S. R. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651–679 (2010).
  CAS PubMed Google Scholar
• Fujii, H. & Zhu, J. K. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc. Natl Acad. Sci. USA 106, 8380–8385 (2009).
  CAS PubMed PubMed Central Google Scholar
• Miyakawa, T., Fujita, Y., Yamaguchi-Shinozaki, K. & Tanokura, M. Structure and function of abscisic acid receptors. Trends Plant Sci. 18, 259–266 (2013).
  CAS PubMed Google Scholar
• Fujita, Y. et al. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17, 3470–3488 (2005).
  CAS PubMed PubMed Central Google Scholar
• Okamoto, M. et al. Activation of dimeric ABA receptors elicits guard cell closure, ABA-regulated gene expression, and drought tolerance. Proc. Natl Acad. Sci. USA 110, 12132–12137 (2013).
  CAS PubMed PubMed Central Google Scholar
• Cao, M. et al. An ABA-mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Res. 23, 1043–1054 (2013).
  CAS PubMed PubMed Central Google Scholar
• González-Guzmán, M. et al. Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance. J. Exp. Bot. 65, 4451–4464 (2014).
  PubMed PubMed Central Google Scholar
• Kim, H. et al. Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression. J. Exp. Bot. 65, 453–464 (2014).
  CAS PubMed PubMed Central Google Scholar
• Park, S. Y. et al. Agrichemical control of plant water use using engineered ABA receptors. Nature http://dx.doi.org/10.1038/nature14123 (2015). Redesign of the ABA-binding pocket of the receptor is achieved to enable activation of the response pathway by another small molecule.
• Thomas, H. & Ougham, H. The stay-green trait. J. Exp. Bot. 65, 3889–3900 (2014).
  CAS PubMed Google Scholar
• De Simone, V., Soccio, M., Borrelli, G. M., Pastore, D. & Trono, D. Stay-green trait-antioxidant status interrelationship in durum wheat (Triticum durum) flag leaf during post-flowering. J. Plant Res. 127, 159–171 (2014).
  PubMed Google Scholar
• Castiglioni, P. et al. Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol. 147, 446–455 (2008).
  CAS PubMed PubMed Central Google Scholar
• Jeong, J. S. et al. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol. 153, 185–197 (2010).
  CAS PubMed PubMed Central Google Scholar
• Qin, H. et al. Regulated expression of an isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions. Plant Cell Physiol. 52, 1904–1914 (2011). Appropriate manipulation of an enzyme in the cytokinin biosynthesis pathway is shown to improve drought tolerance.
  CAS PubMed Google Scholar
• Hasegawa, P. M. Sodium (Na+) homeostasis and salt tolerance of plants. Environ. Exp. Bot. 92, 19–31 (2013).
  CAS Google Scholar
• Platts, B. E. & Grismer, M. E. Chloride levels increase after 13 years of recycled water use in the Salinas Valley. Calif. Agr. 68, 68–74 (2014).
  Google Scholar
• Munns, R. & Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59, 651–681 (2008).
  CAS PubMed Google Scholar
• Deinlein, U. et al. Plant salt-tolerance mechanisms. Trends Plant Sci. 19, 371–379 (2014).
  CAS PubMed PubMed Central Google Scholar
• Schroeder, J. I. et al. Using membrane transporters to improve crops for sustainable food production. Nature 497, 60–66 (2013).
  CAS PubMed PubMed Central Google Scholar
• Roy, S. J., Negrão, S. & Tester, M. Salt resistant crop plants. Curr. Opin. Biotechnol. 26, 115–124 (2014).
  CAS PubMed Google Scholar
• Flowers, T. J. & Colmer, T. D. Salinity tolerance in halophytes. New Phytol. 179, 945–963 (2008).
  CAS PubMed Google Scholar
• Munns, R. et al. Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotech. 30, 360–364 (2012). A Na+-selective transporter located on the plasma membranes of parenchyma cells surrounding the xylem is introduced from a wild relative into wheat and provides significant yield protection in saline soils.
  CAS Google Scholar
• James, R. A. et al. Impact of ancestral wheat sodium exclusion genes Nax1 and Nax2 on grain yield of durum wheat on saline soils. Funct. Plant Biol. 39, 609–618 (2012).
  CAS PubMed Google Scholar
• Dubcovsky, J., María, G. S., Epstein, E., Luo, M. C. & Dvor˘ák, J. Mapping of the K+/Na+ discrimination locus Kna1 in wheat. Theor. Appl. Genet. 92, 448–454 (1996).
  CAS PubMed Google Scholar
• Yang, C. et al. Evolution of physiological responses to salt stress in hexaploid wheat. Proc. Natl Acad. Sci. USA 111, 11882–11887 (2014).
  CAS PubMed PubMed Central Google Scholar
• Ren, Z. H. et al. A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genet. 37, 1141–1146 (2005). Amino acid variations in an HKT-type Na+ transporter associated with enhanced salt tolerance are identified in rice.
  CAS PubMed Google Scholar
• Platten, J. D., Egdane, J. A. & Ismail, A. M. Salinity tolerance, Na+ exclusion and allele mining of HKT1;5 in Oryza sativa and O. glaberrima: many sources, many genes, one mechanism? BMC Plant Biol. 13, 32 (2013).
  CAS PubMed PubMed Central Google Scholar
• Asins, M. J. et al. Two closely linked tomato HKT coding genes are positional candidates for the major tomato QTL involved in Na+/K+ homeostasis. Plant Cell Environ. 36, 1171–1191 (2013).
  CAS PubMed Google Scholar
• Thomson, M. J. et al. Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice 3, 148–160 (2010).
  Google Scholar
• Liu, J., Piñeros, M. A. & Kochian, L. V. The role of aluminum sensing and signaling in plant aluminum resistance. J. Integr. Plant Biol. 56, 221–230 (2014).
  CAS PubMed Google Scholar
• Sasaki, T. et al. Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol. 47, 1343–1354 (2006).
  CAS PubMed Google Scholar
• Sasaki, T. et al. A wheat gene encoding an aluminum-activated malate transporter. Plant J. 37, 645–653 (2004).
  CAS PubMed Google Scholar
• Raman, H. et al. Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor. Appl. Genet. 116, 343–354 (2008).
  CAS PubMed Google Scholar
• Ryan, P. R. et al. The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. Plant J. 64, 446–455 (2010).
  CAS PubMed Google Scholar
• Fujii, M. et al. Acquisition of aluminium tolerance by modification of a single gene in barley. Nature Commun. 3, 713 (2012). Genetic variation in tissue-specific expression of a barley citrate transporter is shown to ameliorate toxicity of aluminium in acid soils.
  Google Scholar
• Magalhaes, J. V. et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genet. 39, 1156–1161 (2007).
  CAS PubMed Google Scholar
• Maron, L. G. et al. Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc. Natl Acad. Sci. USA 110, 5241–5246 (2013). CNV of a malate transporter gene is shown to underlie distinctions in root growth in the presence of high levels of aluminium.
  CAS PubMed PubMed Central Google Scholar
• Li, J. Y. et al. Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc. Natl Acad. Sci. USA 111, 6503–6508 (2014).
  CAS PubMed PubMed Central Google Scholar
• Chatterjee, M. et al. The boron efflux transporter ROTTEN EAR Is required for maize inflorescence development and fertility. Plant Cell 26, 2962–2977 (2014).
  CAS PubMed PubMed Central Google Scholar
• Durbak, A. R. et al. Transport of boron by the tassel-less1 aquaporin is critical for vegetative and reproductive development in maize. Plant Cell 26, 2978–2995 (2014).
  CAS PubMed PubMed Central Google Scholar
• Nable, R. O., Bañuelos, G. S. & Paull, J. G. Boron toxicity. Plant Soil 193, 181–198 (1997).
  CAS Google Scholar
• Sutton, T. et al. Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318, 1446–1449 (2007).
  CAS PubMed Google Scholar
• Schnurbusch, T. et al. Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol. 153, 1706–1715 (2010).
  CAS PubMed PubMed Central Google Scholar
• Pallotta, M. et al. Molecular basis of adaptation to high soil boron in wheat landraces and elite cultivars. Nature 514, 88–91 (2014). Molecular characterization of loci associated with B tolerance uncovers CNV and variation in expression of genes encoding B transporters in wheat cultivars.
  CAS PubMed Google Scholar
• Jones, D. L. et al. Nutrient stripping: the global disparity between food security and soil nutrient stocks. J. Appl. Ecol. 50, 851–862 (2013).
  Google Scholar
• López-Arredondo, D. L., Leyva-González, M. A., González-Morales, S. I., López-Bucio, J. & Herrera-Estrella, L. Phosphate nutrition: improving low-phosphate tolerance in crops. Annu. Rev. Plant Biol. 65, 95–123 (2014).
  PubMed Google Scholar
• Wissuwa, M., Wegner, J., Ae, N. & Yano, M. Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor. Appl. Genet. 105, 890–897 (2002).
  CAS PubMed Google Scholar
• Chin, J. H. et al. Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol. 156, 1202–1216 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hufnagel, B. et al. Duplicate and conquer: multiple homologs of phosphorus-starvation tolerance 1 enhance phosphorus acquisition and sorghum performance on low-P soils. Plant Physiol. 166, 659–677 (2014).
  PubMed PubMed Central Google Scholar
• Miura, K. & Furumoto, T. Cold signaling and cold response in plants. Int. J. Mol. Sci. 14, 5312–5337 (2013).
  CAS PubMed PubMed Central Google Scholar
• Kawamura, Y. & Uemura, M. in Plant Abiotic Stress 2nd edn Ch. 5 (eds Jenks, M. A. & Hasegawa, P. M.) (Wiley, 2014).
  Google Scholar
• Wisniewski, M. et al. Genomics of cold hardiness in woody plants. CRC Crit. Rev. Plant Sci. 33, 92–124 (2014).
  CAS Google Scholar
• Guy, C. Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 187–223 (1990).
  CAS Google Scholar
• Dhillon, T., et al. Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol. 153, 1846–1858 (2010). This is one of several reports describing the functional roles of the key loci that coordinate the acquisition of cold tolerance and transition from vegetative to reproductive growth in temperate cereals.
  CAS PubMed PubMed Central Google Scholar
• Stockinger, E. J., Skinner, J. S., Gardner, K. G., Francia, E. & Pecchioni, N. Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J. 51, 308–321 (2007).
  CAS PubMed Google Scholar
• Knox, A. K. et al. CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor. Appl. Genet. 121, 21–35 (2010).
  PubMed Google Scholar
• Zhu, J. et al. Copy number and haplotype variation at the VRN-A1 and central FR-A2 loci are associated with frost tolerance in hexaploid wheat. Theor. Appl. Genet. 127, 1183–1197 (2014).
  CAS PubMed PubMed Central Google Scholar
• Oliver, S. N., Finnegan, E. J., Dennis, E. S., Peacock, W. J. & Trevaskis, B. Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc. Natl Acad. Sci. USA 106, 8386–8391 (2009).
  CAS PubMed PubMed Central Google Scholar
• Thomashow, M. F. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 154, 571–577 (2010).
  CAS PubMed PubMed Central Google Scholar
• Skinner, J. S. et al. Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol. Biol. 59, 533–551 (2005).
  CAS PubMed Google Scholar
• Badawi, M., Danyluk, J., Boucho, B., Houde, M. & Sarhan, F. The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal _CBF_s. Mol. Genet. Genom. 277, 533–554 (2007).
  CAS Google Scholar
• Francia, E. et al. Two loci on chromosome 5H determine low-temperature tolerance in a 'Nure' (winter) x 'Tremois' (spring) barley map. Theor. Appl. Genet. 108, 670–680 (2004).
  CAS PubMed Google Scholar
• Francia, E. et al. Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor. Appl. Genet. 115, 1083–1091 (2007).
  CAS PubMed Google Scholar
• Dhillon, T. & Stockinger, E. J. Cbf14 copy number variation in the A, B, and D genomes of diploid and polyploid wheat. Theor. Appl. Genet. 126, 2777–2789 (2013).
  CAS PubMed Google Scholar
• Pearce, S. et al. Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat. Theor. Appl. Genet. 126, 2683–2697 (2013).
  PubMed PubMed Central Google Scholar
• Su, C. F. et al. A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol. 153, 145–158 (2010).
  CAS PubMed PubMed Central Google Scholar
• Pachecoy, M. I., Ramirez, I. A., Marín, A. & Pontaroli, A. C. Assessment of cold tolerance at early developmental stages and allelic variation at candidate genes in South American rice germplasm. Euphytica 197, 423–434 (2014).
  CAS Google Scholar
• Yang, Z. et al. Mapping of quantitative trait loci underlying cold tolerance in rice seedlings via high-throughput sequencing of pooled extremes. PLoS ONE 8, e68433 (2013).
  CAS PubMed PubMed Central Google Scholar
• Meng, L. et al. Simultaneous improvement in cold tolerance and yield of temperate japonica rice (Oryza sativa L.) by introgression breeding. Plant Breed. 132, 604–612 (2013).
  CAS Google Scholar
• Peng, S. et al. Rice yields decline with higher night temperature from global warming. Proc. Natl Acad. Sci. USA 101, 9971–9975 (2004).
  CAS PubMed PubMed Central Google Scholar
• Echer, F. R., Oosterhuis, D. M., Loka, D. A. & Rosolem, C. A. High night temperatures during the floral bud stage increase the abscission of reproductive structures in cotton. J. Agron. Crop Sci. 200, 191–198 (2014).
  Google Scholar
• Waters, E. R. The evolution, function, structure, and expression of the plant sHSPs. J. Exp. Bot. 64, 391–403 (2013).
  CAS PubMed Google Scholar
• Lavania, D., Dhingra, A., Siddiqui, M. H., Al-Whaibi, M. H. & Grover, A. Current status of the production of high temperature tolerance transgenic crops for cultivation in warmer climates. Plant Physiol. Biochem. 86, 100–108 (2015).
  CAS PubMed Google Scholar
• Cossani, C. M. & Reynolds, M. P. Physiological traits for improving heat tolerance in wheat. Plant Physiol. 160, 1710–1718 (2012).
  CAS PubMed PubMed Central Google Scholar
• Machado, J. C. et al. Recurrent selection as breeding strategy for heat tolerance in wheat. CBAB 10, 9–15 (2010).
  Google Scholar
• Gororo, N. N., Eagles, H. A., Eastwood, R. F., Nicolas, M. E. & Flood, R. G. Use of Triticum tauschii to improve yield of wheat in low-yielding environments. Euphytica 123, 241–254 (2002).
  Google Scholar
• Benites, F. R. G. & Pinto, C. A. B. P. Genetic gains for heat tolerance in potato in three cycles of recurrent selection. Crop Breed. Appl. Biotechnol. 11, 133–140 (2011).
  Google Scholar
• Mohammed, Y. S. A. et al. Impact of wheat-Leymus racemosus added chromosomes on wheat adaptation and tolerance to heat stress. Breed. Sci. 63, 450–460 (2014).
  CAS PubMed PubMed Central Google Scholar
• Ye, C. et al. Mapping QTL for heat tolerance at flowering stage in rice using SNP markers. Plant Breed. 131, 33–41 (2012).
  CAS Google Scholar
• Shi, W. et al. Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol. 197, 825–837 (2013).
  CAS PubMed Google Scholar
• Ishimaru, T. et al. A genetic resource for early-morning flowering trait of wild rice Oryza officinalis to mitigate high temperature-induced spikelet sterility at anthesis. Ann. Bot. 106, 515–520 (2010).
  PubMed PubMed Central Google Scholar
• Khoury, C. K. et al. An inventory of crop wild relatives of the United States. Crop Sci. 53, 1496–1508 (2013).
  Google Scholar
• Atwell, B. J., Wang, H. & Scafaro, A. P. Could abiotic stress tolerance in wild relatives of rice be used to improve Oryza sativa? Plant Sci. 215–216, 48–58 (2014).
  PubMed Google Scholar
• Prasanna, B. M. Diversity in global maize germplasm: characterization and utilization. J. Biosci. 37, 843–855 (2012).
  CAS PubMed Google Scholar
• Qi, X. et al. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nature Commun. 5, 4340 (2014).
  CAS Google Scholar
• Bolger, A. et al. The genome of the stress-tolerant wild tomato species Solanum pennellii. Nature Genet. 46, 1034–1038 (2014).
  CAS PubMed Google Scholar
• Furuta, T. et al. Development and evaluation of chromosome segment substitution lines (CSSLs) carrying chromosome segments derived from Oryza rufipogon in the genetic background of Oryza sativa L. Breed. Sci. 63, 468–475 (2014).
  CAS PubMed PubMed Central Google Scholar
• Baltazar, M. D. et al. QTL mapping for tolerance of anaerobic germination from IR64 and the aus landrace Nanhi using SNP genotyping. Euphytica 197, 251–260 (2014).
  CAS Google Scholar
• Oh, D. H. et al. Genome structures and transcriptomes signify niche adaptation for the multiple-ion-tolerant extremophyte Schrenkiella parvula. Plant Physiol. 164, 2123–2138 (2014).
  CAS PubMed PubMed Central Google Scholar
• Li, X. L., Yang, X., Hu, Y. X., Yu, X. D. & Li, Q. L. A novel NAC transcription factor from Suaeda liaotungensis K. enhanced transgenic Arabidopsis drought, salt, and cold stress tolerance. Plant Cell Rep. 33, 767–778 (2014).
  CAS PubMed Google Scholar
• Leiser, W. L. et al. Two in one sweep: aluminum tolerance and grain yield in P-limited soils are associated to the same genomic region in West African sorghum. BMC Plant Biol. 14, 206 (2014).
  PubMed PubMed Central Google Scholar
• Topp, C. N. et al. 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. Proc. Natl Acad. Sci. USA 110, E1695–E1704 (2013).
  CAS PubMed PubMed Central Google Scholar
• Araus, J. L. & Cairns, J. E. Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci. 19, 52–61 (2014).
  CAS PubMed Google Scholar
• Zhang, Y. et al. Transcription activator-like effector nucleases enable efficient plant genome engineering. Plant Physiol. 161, 20–27 (2013).
  CAS PubMed Google Scholar
• Zhang, H. et al. The CRISPR/Cas9 system produces specific and homozygous targeted gene editing in rice in one generation. Plant Biotechnol. J. 12, 797–807 (2014).
  CAS PubMed Google Scholar
• Cotsaftis, O., Plett, D., Shirley, N., Tester, M. & Hrmova, M. A two-staged model of Na+ exclusion in rice explained by 3D modeling of HKT transporters and alternative splicing. PLoS ONE 7, e39865 (2012).
  CAS PubMed PubMed Central Google Scholar
• Byrt, C. S. et al. HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol. 143, 1918–1928 (2007).
  CAS PubMed PubMed Central Google Scholar
• Zhou, G. et al. Enhancing the aluminium tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. J. Exp. Bot. 65, 2381–2390 (2014).
  CAS PubMed PubMed Central Google Scholar
• Pariasca-Tanaka, J. et al. A novel allele of the P-starvation tolerance gene OsPSTOL1 from African rice (Oryza glaberrima Steud) and its distribution in the genus Oryza. Theor. Appl. Genet. 127, 1387–1398 (2014).
  CAS PubMed PubMed Central Google Scholar
• Ainsworth, E. A., Yendrek, C. R., Sitch, S., Collins, W. J. & Emberson, L. D. The effects of tropospheric ozone on net primary productivity and implications for climate change. Annu. Rev. Plant Biol. 63, 637–661 (2012).
  CAS PubMed Google Scholar
• Uauy, C., Distelfeld, A., Fahima, T., Blechl, A. & Dubcovsky, J. A. NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298–1301 (2006).
  CAS PubMed PubMed Central Google Scholar