Heat stress regimes for the investigation of pollen thermotolerance in crop plants

Plant Reproduction

Volumn 29, Issue 1-2, 2016, Pages 93-105

  Mesihovic, Anida ^a   Iannacone, Rina ^b   Firon, Nurit ^c   Fragkostefanakis, Sotirios ^a  

^a GOETHE UNIVERSITY   (Germany)

^b ALSIA Research Center Metapontum Agrobios Metaponto (MT)   (Italy)

^c VOLCANI CENTER   (Israel)

Author keywords

Anther; Crop; Heat stress; Mild chronic; Pollen; Thermotolerance

Indexed keywords

CROP; HEAT; HEAT TOLERANCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POLLEN;

CROPS, AGRICULTURAL; HOT TEMPERATURE; POLLEN; STRESS, PHYSIOLOGICAL; THERMOTOLERANCE;

EID: 84961675291     PISSN: 21947953     EISSN: 21947961     Source Type: Journal    
DOI: 10.1007/s00497-016-0281-y     Document Type: Review

References (114)

1. Abdul-baki AA (1992) Determination of pollen viability in tomatoes. J Am Soc Hortic Sci 117:473–476
2. Abdul-Baki A, Stommel JR (1995) Pollen viability and fruit set of tomato genotypes under optimum-and high-temperature regimes. HortScience 30:115–117
3. Abou-Shleel E-S (2014) GIS assessment of climate change impacts on tomato crop in Egypt National Authority for Remote Sensing and Space Sciences (NARSS). Egypt. 8:26–34. doi:10.5829/idosi.gjer.2014.8.2.854
4. Ahmed FE, Hall AE, DeMason DA (1992) Heat injury during floral development in Cowpea (Vigna unguiculata, Fabaceae). Am J Bot 79:784. doi:10.2307/2444945
5. Aloni B, Peet M, Pharr M, Karni L (2001) The effect of high temperature and high atmospheric CO2 on carbohydrate changes in bell pepper (Capsicum annuum) pollen in relation to its germination. Physiol Plant 112:505–512. doi:10.1034/j.1399-3054.2001.1120407.x
6. Baker JT, Allen LH, Boote KJ (1992) Temperature effects on rice at elevated CO2 concentration. J Exp Bot 43:959–964. doi:10.1093/jxb/43.7.959
7. Barnabás B, Jäger K, Fehér A (2007) The effect of drought and heat stress on reproductive processes in cereals. Plant, Cell Environ. doi:10.1111/j.1365-3040.2007.01727.x
8. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4:879–887. doi:10.1105/tpc.4.8.879
9. Bianchini M, Pacini E (1966) Explosive anther dehiscence in Ricinus communis L. involves cell wall modifications and relative humidity. Int J Plant Sci 157:739–745
10. Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273. doi:10.3389/fpls.2013.00273
11. Bokszczanin KL, Fragkostefanakis S (2013) Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci 4:315. doi:10.3389/fpls.2013.00315
12. Calderini DF, Savin R, Slafer GA, Abeledo LG (1999) Final grain weight in wheat as affected by short periods of high temperature during pre- and post-anthesis under field conditions. Aust J Plant Physiol 26:453. doi:10.1071/PP99015
13. Camejo D, Rodríguez P, Angeles Morales M et al (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol 162:281–289. doi:10.1016/j.jplph.2004.07.014
14. Charng Y, Liu H, Liu N et al (2006) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143:251–262. doi:10.1104/pp.106.091322
15. Comlekcioglu N, Soylu MK (2010) Determination of high temperature tolerance via screening of flower and fruit formation in tomato. Yyu J Agric Sci 20:123–130
16. Dane F, Gene Hunter A, Chambliss OL (1991) Fruit set, pollen fertility, and combining ability of selected tomato genotypes under high-temperature field conditions. J Am Soc Hortic Sci 116:906–910
17. Das S, Krishnan P, Nayak M, Ramakrishnan B (2014) High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes. Environ Exp Bot 101:36–46. doi:10.1016/j.envexpbot.2014.01.004
18. Dupuis L, Dumas C (1990) Influence of temperature stress on in vitro fertilization and heat shock protein synthesis in maize (Zea mays L.) reproductive systems. Plant Physiol 94:665–670
19. Endo M, Tsuchiya T, Hamada K et al (2009) High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol 50:1911–1922. doi:10.1093/pcp/pcp135
20. Evans LT (1978) The influence of irradiance before and after anthesis on grain yield and its components in microcrops of wheat grown in a constant daylength and temperature regime. Field Crop Res 1:5–19. doi:10.1016/0378-4290(78)90003-5
21. Farooq M, Bramley H, Palta JA, Siddique KHM (2011) Heat stress in wheat during reproductive and grain-filling phases. CRC Crit Rev Plant Sci 30:491–507. doi:10.1080/07352689.2011.615687
22. Firon N, Shaked R, Peet MM et al (2006) Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions. Sci Hortic (Amst) 109:212–217. doi:10.1016/j.scienta.2006.03.007
23. Firon N, Nepi M, Pacini E (2012a) Water status and associated processes mark critical stages in pollen development and functioning. Ann Bot 109:1201–1214. doi:10.1093/aob/mcs070
24. Firon N, Pressman E, Meir S et al (2012b) Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants. doi:10.1093/aobpla/pls024
25. Fragkostefanakis S, Simm S, Paul P et al (2014) Chaperone network composition in Solanum lycopersicum explored by transcriptome profiling and microarray meta-analysis. Plant, Cell Environ. doi:10.1111/pce.12426
26. Fragkostefanakis S, Röth S, Schleiff E, Scharf K-D (2015) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant, Cell Environ 38:1881–1895. doi:10.1111/pce.12396
27. Fragkostefanakis S, Mesihovic A, Simm S et al (2016) HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol. doi:10.1104/pp.15.01913
28. Frank G, Pressman E, Ophir R et al (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908. doi:10.1093/jxb/erp234
29. Fukai S, Cooper M (1995) Development of drought-resistant cultivars using physio-morphological traits in rice. F Crop Res 40:67–86. doi:10.1016/0378-4290(94)00096-U
30. Geisenberg C, Stewart K (1986) Field crop management. In: Atherton J, Rudich J (eds) The tomato crop. Springer, Amsterdam, pp 511–557
31. Giorno F, Wolters-Arts M, Mariani C, Rieu I (2013) Ensuring reproduction at high temperatures: the heat stress response during anther and pollen development. Plants 2:489–506. doi:10.3390/plants2030489
32. Gote GN, Padghan PR (2009) Studies on different thermal regimes and thermal sensitivity analysis of tomato genotypes. Asian J Environ Sci 3:158–161
33. Gradziel TM, Weinbaum SA (1999) High relative humidity reduces anther dehiscence in apricot, peach, and almond. HortScience 34:322–325
34. Gross Y, Kigel J (1994) Differential sensitivity to high temperature of stages in the reproductive development of common bean (Phaseolus vulgaris L.). Field Crop Res 36:201–212. doi:10.1016/0378-4290(94)90112-0
35. Hansen G (2015) The evolution of the evidence base for observed impacts of climate change. Curr Opin Environ Sustain. doi:10.1016/j.cosust.2015.05.005
36. Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extremes. doi:10.1016/j.wace.2015.08.001
37. 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 Physiol 116:439–444. doi:10.1104/pp.116.1.439
38. Hedhly A (2011) Sensitivity of flowering plant gametophytes to temperature fluctuations. Environ Exp Bot 74:9–16. doi:10.1016/j.envexpbot.2011.03.016
39. Hedhly A, Hormaza JI, Herrero M (2005) Influence of genotype-temperature interaction on pollen performance. J Evol Biol 18:1494–1502. doi:10.1111/j.1420-9101.2005.00939.x
40. Herrero M, Hormaza JI (1996) Pistil strategies controlling pollen tube growth. Sex Plant Reprod 9:343–347. doi:10.1007/s004970050053
41. Herrero P, Johnson RR (1980) High temperature stress and pollen viability of maize. Crop Sci 20:796–800. doi:10.2135/cropsci1980.0011183X002000060030x
42. Honys D, Renak D, Twell D (2006) Male gametophyte development and function. Floric Ornam Plant Biotechnol Adv Top Issues 1:76–87
43. 2 and global climate change on rice yield in Japan. In: Omasa K, Kai K, Taoda H, Uchijima Z, Yoshino M (eds) Climate change and plants in East Asia. Springer, Tokyo, pp 39–56
44. IPCC (2014) Climate Change 2014 synthesis report summary chapter for policymakers. IPCC 31. doi:10.1017/CBO9781107415324
45. Ishimaru T, Hirabayashi H, Ida M et al (2010) 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. doi:10.1093/aob/mcq124
46. Iwahori S (1965) High temperature injuries in tomato. IV. Engei Gakkai zasshi 34:33–41. doi:10.2503/jjshs.34.33
47. Jagadish SVK, Craufurd PQ, Wheeler TR (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot 58:1627–1635. doi:10.1093/jxb/erm003
48. Jäger K, Fábián A, Barnabás B (2008) Effect of water deficit and elevated temperature on pollen development of drought sensitive and tolerant winter wheat (Triticum aestivum L.) genotypes. Acta Biol Szeged 52:67–71
49. Karapanos IC, Akoumianakis KA, Olympios CM, Passam HC (2010) Tomato pollen respiration in relation to in vitro germination and pollen tube growth under favourable and stress-inducing temperatures. Sex Plant Reprod 23:219–224. doi:10.1007/s00497-009-0132-1
50. 2 concentration and high temperature on growth and yield of rice: I. The effect on development, dry matter production and some growth characteristics. Jpn J Crop Sci 65:634–643. doi:10.1626/jcs.65.634
51. Kim J, Shon J, Lee CK et al (2011) Relationship between grain filling duration and leaf senescence of temperate rice under high temperature. Field Crop Res 122:207–213. doi:10.1016/j.fcr.2011.03.014
52. Kotak S, Larkindale J, Lee U et al (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316. doi:10.1016/j.pbi.2007.04.011
53. Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010) What is stress? Concepts, definitions and applications in seed science. New Phytol 188:655–673. doi:10.1111/j.1469-8137.2010.03461.x
54. Lämke J, Brzezinka K, Altmann S, Bäurle I (2015) A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. doi:10.15252/embj.201592593
55. Larkindale J, Vierling E (2007) Core genome responses involved in acclimation to high temperature. Plant Physiol 146:748–761. doi:10.1104/pp.107.112060
56. Larkindale J, Hall JD, Knight MR et al (2005) Heat stress phenotypes of arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897. doi:10.1104/pp.105.062257.882
57. Li S, Fu Q, Chen L et al (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233:1237–1252. doi:10.1007/s00425-011-1375-2
58. Lobell DB, Ortiz-Monasterio JI, Asner GP et al (2005) Analysis of wheat yield and climatic trends in Mexico. Field Crop Res 94:250–256. doi:10.1016/j.fcr.2005.01.007
59. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620. doi:10.1126/science.1204531
60. Lyakh VA, Kravchenko AN, Soroka AI, Dryuchina EN (1991) Effects of high temperatures on mature pollen grains in wild and cultivated maize accessions. Euphytica 55:203–207. doi:10.1007/BF00021240
61. Mascarenhas JP, Crone DE (1996) Pollen and the heat shock response. Sex Plant Reprod 9:370–374. doi:10.1007/BF02441959
62. Matsui T (1999) Mechanism of anther dehiscence in Rice (Oryza sativa L.). Ann Bot 84:501–506. doi:10.1006/anbo.1999.0943
63. Matsui T, Omasa K (2002) Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Ann Bot 89:683–687. doi:10.1093/aob/mcf112
64. Matsui T, Omasa K, Horie T (1999) Rapid swelling of pollen grains in response to floret opening unfolds anther locules in rice (Oryza sativa L.). Plant Prod Sci 2:196–199. doi:10.1626/pps.2.196
65. Matsui T, Omasa K, Horie T (2001) The difference in sterility due to high temperatures during the flowering period among Japonica-rice varieties. Plant Prod Sci 4:90–93. doi:10.1626/pps.4.90
66. Matsui T, Kobayasi K, Kagata H, Horie T (2005) Correlation between viability of pollination and length of basal dehiscence of the theca in rice under a hot-and-humid condition. Plant Prod Sci 8:109–114. doi:10.1626/pps.8.109
67. Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125. doi:10.1016/j.tibs.2011.11.007
68. Mohammed AR, Tarpley L (2009) High nighttime temperatures affect rice productivity through altered pollen germination and spikelet fertility. Agric For Meteorol 149:999–1008. doi:10.1016/j.agrformet.2008.12.003
69. Monterroso VA, Wien HC (1990) Flower and pod abscission due to heat stress in beans. J Am Soc Hortic Sci 115:631–634
70. Nover L (1991) Heat shock response. CRC Press, Boca Raton
71. Peet MM, Willits DH, Gardner R (1997) Response of ovule development and post-pollen production processes in male-sterile tomatoes to chronic, sub-acute high temperature stress. J Exp Bot 48:101–111. doi:10.1093/jxb/48.1.101
72. Peet MM, Sato S, Gardner RG (1998) Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant, Cell Environ 21:225–231. doi:10.1046/j.1365-3040.1998.00281.x
73. Peng S, Huang J, Sheehy JE et al (2004) Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101:9971–9975. doi:10.1073/pnas.0403720101
74. Porch TG, Jahn M (2001) Effects of high-temperature stress on microsporogenesis in heat-sensitive and heat-tolerant genotypes of Phaseolus vulgaris. Plant, Cell Environ 24:723–731. doi:10.1046/j.1365-3040.2001.00716.x
75. Prasad PVV, Craufurd PQ, Summerfield (1999) Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress. Ann Bot 84:381–386. doi:10.1006/anbo.1999.0926
76. Prasad PVV, Boote KJ, Allen LH et al (2006a) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crop Res 95:398–411. doi:10.1016/j.fcr.2005.04.008
77. Prasad PVV, Boote KJ, Allen LH (2006b) Adverse high temperature effects on pollen viability, seed-set, seed yield and harvest index of grain-sorghum [Sorghum bicolor (L.) Moench] are more severe at elevated carbon dioxide due to higher tissue temperatures. Agric For Meteorol 139:237–251. doi:10.1016/j.agrformet.2006.07.003
78. Prasad PVV, Pisipati SR, Ristic Z et al (2008) Impact of nighttime temperature on physiology and growth of spring wheat. Crop Sci 48:2372. doi:10.2135/cropsci2007.12.0717
79. Pressman E (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Ann Bot 90:631–636. doi:10.1093/aob/mcf240
80. Queitsch C, Hong SW, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479–492. doi:10.1105/tpc.12.4.479
81. Rao BB, Chowdary PS, Sandeep VM et al (2015) Spatial analysis of the sensitivity of wheat yields to temperature in India. Agric For Meteorol 200:192–202. doi:10.1016/j.agrformet.2014.09.023
82. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253–266. doi:10.1016/j.molcel.2010.10.006
83. Rizhsky L, Liang H, Shuman J et al (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696. doi:10.1104/pp.103.033431.1
84. Rudich J, Zamski E, Regev Y (1977) Genotypic variation for sensitivity to high temperature in the tomato: pollination and fruit set. Bot Gaz 138:448–452
85. Saini HS, Aspinall D (1982) Abnormal sporogenesis in Wheat (Triticum aestivum L.) Induced by short periods of high temperature. Ann Bot 49:835–846
86. Saini HS, Sedgley M, Aspinall D (1984) Developmental anatomy in wheat of male sterility induced by heat stress, water deficit or abscisic acid. Aust J Plant Physiol 11:243–253. doi:10.1071/PP9840243
87. Sakata T, Takahashi H, Nishiyama I, Higashitani A (2000) Effects of high temperature on the development of pollen mother cells and microspores in barley Hordeum vulgare L. J Plant Res 113:395–402. doi:10.1007/PL00013947
88. Satake T, Yoshida S (1978) High temperature-induced sterility in indica rices at flowering. Jpn J Crop Sci 47:6–17
89. Sato S (2006) Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development. Ann Bot 97:731–738. doi:10.1093/aob/mcl037
90. Sato S, Peet MM, Thomas JF (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant, Cell Environ 23:719–726. doi:10.1046/j.1365-3040.2000.00589.x
91. Sato S, Peet MM, Thomas JF (2002) Determining critical pre-and post-anthesis periods and physiological processes in Lycopersicon esculentum Mill. exposed to moderately elevated temperatures. J Exp Bot 53:1187–1195
92. Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant, Cell Environ 28:269–277. doi:10.1111/j.1365-3040.2005.01324.x
93. Shen H, Zhong X, Zhao F et al (2015) Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nat Biotechnol 33:1–11. doi:10.1038/nbt.3321
94. Snider JL, Oosterhuis DM (2011) How does timing, duration, and severity of heat stress influence pollen–pistil interactions in angiosperms? Plant Signal Behav 6:930–933. doi:10.4161/psb.6.7.15315
95. Stone P, Nicolas M (1995) A survey of the effects of high temperature during grain filling on yield and quality of 75 wheat cultivars. Aust J Agric Res 46:475–492. doi:10.1071/AR9950475
96. Sung DY, Kaplan F, Lee KJ, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8:179–187. doi:10.1016/S1360-1385(03)00047-5
97. Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11:515–528. doi:10.1038/nrm2918
98. Trivedi AK (2015) Adaptations and mechanisms of heat stress tolerance of plants. Academic Res J Agric Sci Res 3:151–160. doi:10.14662/ARJASR2015.036
99. Vierling E (1991) The roles of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620. doi:10.1146/annurev.pp.42.060191.003051
100. Wahid A, Gelani S, Ashraf M, Foolad M (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223. doi:10.1016/j.envexpbot.2007.05.011
101. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252. doi:10.1016/j.tplants.2004.03.006
102. Warrag MOA, Hall AE (1984a) Reproductive responses of cowpea (Vigna unguiculata (L.) Walp.) to heat stress. II. Responses to night air temperature. Field Crop Res 8:17–33. doi:10.1016/0378-4290(84)90049-2
103. Warrag MOA, Hall AE (1984b) Reproductive responses of cowpea (Vigna unguiculata L.). Field Crop Res 8:17–33. doi:10.1016/0378-4290(84)90048-0
104. Warrington IJ, Dustone RL, Green LM (1977) Temperature effects at three development stages on the yield of the wheat ear. Aust J Agric Res 28:11–27. doi:10.1071/AR9770011
105. Welch JR, Vincent JR, Auffhammer M et al (2010) Rice yields in tropical/subtropical Asia exhibit large but opposing sensitivities to minimum and maximum temperatures. Proc Natl Acad Sci USA 107:14562–14567. doi:10.1073/pnas.1001222107
106. Wheeler T, Craufurd PQ, Ellis RH et al (2000) Temperature variability and the yield of annual crops. Agric Ecosyst Environ 82:159–167. doi:10.1016/S0167-8809(00)00224-3
107. Willits DH, Peet MM (1998) The effect of night temperature on greenhouse grown tomato yields in warm climates. Agric For Meteorol 92:191–202. doi:10.1016/S0168-1923(98)00089-6
108. Wollenweber B, Porter JR, Schellberg J (2003) Lack of interaction between extreme high-temperature events at vegetative and reproductive growth stages in wheat. J Agron Crop Sci 189:142–150. doi:10.1046/j.1439-037X.2003.00025.x
109. Yates I, Sparks D (1993) Environmental regulation of anther dehiscence and pollen germination in pecan. J Am Soc 118:699–706
110. Yeh C-H, Kaplinsky NJ, Hu C, Charng Y-Y (2012) Some like it hot, some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci 195:10–23. doi:10.1016/j.plantsci.2012.06.004
111. Young LW, Wilen RW, Bonham-Smith PC (2004) High temperature stress of Brassica napus during flowering reduces micro- and megagametophyte fertility, induces fruit abortion, and disrupts seed production. J Exp Bot 55:485–495. doi:10.1093/jxb/erh038
112. Zhang X, Li J, Liu A et al (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS ONE. doi:10.1371/journal.pone.0049652
113. Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot 61:1959–1968. doi:10.1093/jxb/erq053
114. 2 and temperature: growth and yield response of 17 cultivars. J Exp Bot 1(47):1353–1359