Quantifying the relationship between temperature regulation in the ear and floret development stage in wheat (Triticum aestivum L.) under heat and drought stress
Frederick T. Steinmeyer A , Martin Lukac A , Matthew P. Reynolds B and Hannah E. Jones A CA School of Agriculture, Policy and Development, University of Reading, Reading RG6 6AR, UK.
B International Maize and Wheat Improvement Centre, Int. AP 6-641, 06600 Mexico DF, Mexico.
C Corresponding author. Email: h.e.jones@reading.ac.uk
Functional Plant Biology 40(7) 700-707 https://doi.org/10.1071/FP12362
Submitted: 4 December 2012 Accepted: 15 April 2013 Published: 6 June 2013
Abstract
Thermal imaging is a valuable tool for the clarification of gas exchange dynamics between a plant and its environment. The presence of stomata in wheat (Triticum aestivum L.) glumes and awns offers an opportunity to assess the photosynthetic activity of ears up to and during flowering. Knowledge of the spatial and temporal thermodynamics of the wheat ear may provide insight into interactions between floret developmental stage (FDS), temperature depression (TD) and ambient environment, with potential to use these as high-throughput screening tools for breeders. A controlled environment study was conducted using six spring wheat genotypes of the elite recombinant inbred line Seri–Babax. Average ear temperature was recorded using a hand-held infrared camera and gas exchange was measured by enclosing ears in a custom-built cuvette. FDS was monitored and recorded daily throughout the study. Plants were grown in pots and exposed to a combination of two temperature and two water regimes. In the studied wheat lines, TD varied from 0.1°C to 0.6°C according to the level of stress imposed. The results indicated that TD does not occur at FDS F3, the peak of active flowering, but during the stages before pollen release and stigma maturity (F1–F2). These findings suggest that ear temperature during the early stages of anthesis, before pollen release and full extension of the stigma, are likely to be the most relevant for identifying heat stress tolerant genotypes.
Additional keywords: anthesis, controlled environment, screening, temperature depression.
References
Acevedo E, Silva P, Silva H (2002) Wheat growth and physiology. In ‘Bread wheat: improvement and production’. (Eds BC Curtis, S Rajaram, H Gómez Macpherson). pp. 53–89.(Food and Agriculture Organisation: Rome)Al-Khatib K, Paulsen GM (1984) Mode of high temperature injury to wheat during grain development. Journal of Plant Physiology 61, 363–368.
| Mode of high temperature injury to wheat during grain development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1OnsLo%3D&md5=9d01eeb5c01c92adc2996e8d725ef3dfCAS |
Bahar B, Yildirim M, Barutcular C, Genc I (2008) Effect of canopy temperature depression on grain yield and grain components in bread and durum wheat. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 36, 34–37.
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
| Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |
Bita CE, Zenoni S, Vriezen WH, Mariani C, Pezzotti M, Gerats T (2011) Temperature stress differentially modulates transcription in meiotic anthers of heat-tolerant and heat-sensitive tomato plants. BMC Genomics 12, 384
| Temperature stress differentially modulates transcription in meiotic anthers of heat-tolerant and heat-sensitive tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtV2mtb7F&md5=0ab59be43ef9510bac39a6f33b34469dCAS | 21801454PubMed |
Blum A (1985) Photosynthesis and transpiration in leaves and ears of wheat and barley varieties. Journal of Experimental Botany 36, 432–440.
| Photosynthesis and transpiration in leaves and ears of wheat and barley varieties.Crossref | GoogleScholarGoogle Scholar |
Blum A (1986) The effect of heat stress on wheat leaf and ear photosynthesis. Journal of Experimental Botany 37, 111–118.
| The effect of heat stress on wheat leaf and ear photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Blum A (1988) ‘Plant breeding for stress environments.’ (CRC Press: Boca Raton)
Blum A, Mayer J, Gozlan G (1982) Infrared thermal sensing of plant canopies as a screening technique for dehydration avoidance in wheat. Field Crops Research 5, 137–146.
| Infrared thermal sensing of plant canopies as a screening technique for dehydration avoidance in wheat.Crossref | GoogleScholarGoogle Scholar |
Blum A, Shipiler L, Golan G, Mayer J (1989) Yield stability and canopy temperature of wheat genotypes under drought stress. Field Crops Research 22, 289–296.
| Yield stability and canopy temperature of wheat genotypes under drought stress.Crossref | GoogleScholarGoogle Scholar |
Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of limid transfer protein in response to periodic drying events in leaves of tree tobacco. Journal of Plant Physiology 140, 176–183.
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany 103, 551–560.
| Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7s%3D&md5=c0a3d54246b0668e76fa3410ea5d90a2CAS | 18662937PubMed |
Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity in pollination. The Plant Cell 16, S84–S97.
| Pollen and stigma structure and function: the role of diversity in pollination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsFWltLo%3D&md5=c233aad4606c6626c5bd64c225d76a6aCAS | 15075396PubMed |
Evans LT, Bingham J, Johnson P, Sutherland J (1972) Effect of awns and drought on the supply of photosynthate and its distribution within wheat ears. Annals of Applied Biology 70, 67–76.
| Effect of awns and drought on the supply of photosynthate and its distribution within wheat ears.Crossref | GoogleScholarGoogle Scholar |
Fischer RA, Rees D, Sayre KD, Lu Z-M, Condon AG, Larqué-Saavedra A (1998) Wheat yield progress is associated with higher stomatal conductance and photosynthetic rate, and cooler canopies. Journal of Crop Science 38, 1467–1475.
| Wheat yield progress is associated with higher stomatal conductance and photosynthetic rate, and cooler canopies.Crossref | GoogleScholarGoogle Scholar |
FLIR (2013) FLIR T-Series specifications (T335). (FLIR: Oregon, USA) Available online at: http://www.flir.com/cs/emea/en/view/?id=41969 [Verified 7 May 2013]
Fox P, López C, Skovmand B, Sánchez H, Herrera R, White JW, Duveiller E, van Ginkel M (1996) ‘International wheat information system (IWIS). Vol. 1.’ (International Maize and Wheat Improvement Centre: Mexico City)
Graham AW, McDonald GK (2001) Effects of zinc on photosynthesis and yield of wheat under heat stress. In ‘Proceedings of the 10th Australian Agronomy Conference,’ January 2001, Hobart, Tasmania.
Hsiao TC, O’Toole JC, Yambao EB, Turner NC (1984) Influence of osmotic adjustment on leaf rolling and tissue death in rice (Oryza sativa L.). Journal of Plant Physiology 75, 338–341.
| Influence of osmotic adjustment on leaf rolling and tissue death in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhsFOqsQ%3D%3D&md5=bac4972f30555144298d2fa40ad4d33aCAS |
Hurd EA (1968) Growth of roots of seven cultivars of spring wheat at high and low moisture levels. Agronomy Journal 60, 201–205.
| Growth of roots of seven cultivars of spring wheat at high and low moisture levels.Crossref | GoogleScholarGoogle Scholar |
International Maize and Wheat Improvement Centre (CIMMYT) Wheat Personnel (1986) ‘Veery ‘S’: bread wheats for many environments.’ (CIMMYT: Mexico City)
Karimizadeh R, Mohammadi M (2011) Association of canopy temperature depression with yield of durum wheat genotypes under supplementary irrigated and rainfed conditions. Australian Journal of Crop Science 5, 138–146.
Keijzer CJ, Leferink-Ten Klooster HB, Reinders MC (1996) The mechanisms of the grass flower: anther dehiscence and pollen shedding in maize. Annals of Botany 78, 15–21.
| The mechanisms of the grass flower: anther dehiscence and pollen shedding in maize.Crossref | GoogleScholarGoogle Scholar |
Lawlor DW (2009) Musings about the effects of environment on photosynthesis. Annals of Botany 103, 543–549.
| Musings about the effects of environment on photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGnu7o%3D&md5=c604c10432e924a95dc782886db9c5efCAS | 19205084PubMed |
Lopes MS, Reynolds MP (2010) Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat. Functional Plant Biology 37, 147–156.
| Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat.Crossref | GoogleScholarGoogle Scholar |
Lu C, Zang J (2000) Heat-induced multiple effects on PSII in wheat plants. Journal of Plant Physiology 156, 259–265.
| Heat-induced multiple effects on PSII in wheat plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1yitLY%3D&md5=dacd2bac062f195f5dd57b0c41e9d457CAS |
Lukac M, Gooding MJ, Griffiths S, Jones HE (2012) Asynchronous flowering and within-plant flowering diversity in wheat and the implications for crop resilience to heat. Annals of Botany 109, 843–850.
| Asynchronous flowering and within-plant flowering diversity in wheat and the implications for crop resilience to heat.Crossref | GoogleScholarGoogle Scholar | 22186277PubMed |
Matsui T, Omassa K, Horie T (2000) High temperature at flowering inhibit swelling of pollen grains, a driving force for anther dehiscence in rice (Oryza sativa L.). Plant Production Science 3, 430–434.
| High temperature at flowering inhibit swelling of pollen grains, a driving force for anther dehiscence in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar |
McDaniel RG (1982) The physiology of temperature effects on plants. In ‘Breeding plants for less favorable environments’. (Eds. MN Christiansen MN, CF Lewis) pp. 13–45. (Wiley: New York)
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVKjsw%3D%3D&md5=ebbf428bd1a356e9c1d2601ae45d60adCAS | 16359910PubMed |
Morgan MJ, Condon AG (1986) Water-use, grain yield and osmoregulation in wheat. Australian Journal of Plant Physiology 35, 299–319.
Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. The Plant Journal 29, 743–750.
| Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs12msr4%3D&md5=525f195d31de026a007102aca684e1e0CAS | 12148532PubMed |
Nevo E, Ordentlich A, Beiles A, Raskin I (1992) Genetic divergence of heat production within and between wild progenitors of wheat and barley: evolutionary and agronomical implications. Journal of Theoretical Applied Genetics 84, 958–962.
Olivares-Villegas JJ, Reynolds MP, McDonald GK (2007) Drought-adaptive attributes in the Seri/Babax hexaploid wheat population. Functional Plant Biology 34, 189–203.
| Drought-adaptive attributes in the Seri/Babax hexaploid wheat population.Crossref | GoogleScholarGoogle Scholar |
Parry MA, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu XG, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. Journal of Experimental Botany 62, 453–467.
| Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFyrsbrO&md5=df4842d655dde29d4fc2f3b3f7ed0076CAS | 21030385PubMed |
Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (Eds.). (2007) ‘Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the fourth assessment report of the Intergovernmental Panel on Climate Change.’ (Cambridge University Press: Cambridge, UK)
Pfeiffer WH (1998) Drought tolerance in bread wheat – analysis of yield improvement over the years in CIMMYT germplasm. In ‘Wheat production constraints in tropical environments. Proceedings of the international conference’. (Ed. AR Klatt) pp. 274–284. (International Maize and Wheat Improvement Centre: Mexico City)
Pinto RS, Reynolds MP, Mathews KL, McIntyre CL, Olivares-Villegas JJ, Chapman SC (2010) Heat and drought adaptive QTL in a wheat population designed to minimize confounding agronomic effects. Theoretical and Applied Genetics 121, 1001–1021.
| Heat and drought adaptive QTL in a wheat population designed to minimize confounding agronomic effects.Crossref | GoogleScholarGoogle Scholar | 20523964PubMed |
Prasad VP, Craufurd PQ, Summerfield RJ (1999) Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress. Annals of Botany 84, 381–386.
| Fruit number in relation to pollen production and viability in groundnut exposed to short episodes of heat stress.Crossref | GoogleScholarGoogle Scholar |
Reynolds M (2002) Physiological approaches to wheat breeding. In ‘Bread wheat: improvement and production’. (Eds BC Curtis, S Rajaram S, H Gómez Macpherson) pp. 143–165. (Food and Agriculture Organisation: Rome)
Reynolds MP, Singh RP, Ibrahim A, Agreeb OAA, Larque Saavedra A, Quick JS (1998) Evaluating physiological traits to compliment empirical selection for wheat in warm environments. Euphytica 100, 85–94.
| Evaluating physiological traits to compliment empirical selection for wheat in warm environments.Crossref | GoogleScholarGoogle Scholar |
Saini HS, Aspinall D (1982) Abnormal sporogenesis in wheat (Triticum aestivum L.) induced by short periods of high temperature. Annals of Botany 49, 835–846.
Saini HS, Sedgely M, Aspinall D (1983) Effect of heat stress during floral development on pollen tube growth and ovary anatomy in wheat (Triticum aestivum L.). Australian Journal of Plant Physiology 10, 137–144.
| Effect of heat stress during floral development on pollen tube growth and ovary anatomy in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Teare ID, Law AG, Simmons GF (1972) Stomatal frequency and distribution on the inflorescence of Triticum aestivum. Canadian Journal of Plant Science 52, 89–94.
| Stomatal frequency and distribution on the inflorescence of Triticum aestivum.Crossref | GoogleScholarGoogle Scholar |
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
| Heat tolerance in plants: an overview.Crossref | GoogleScholarGoogle Scholar |
Waite R, Boyd J (1953) The water-soluble carbohydrates of grasses. I. Changes occurring during the normal life-cycle. Journal of the Science of Food and Agriculture 4, 197–204.
| The water-soluble carbohydrates of grasses. I. Changes occurring during the normal life-cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG3sXjsFanug%3D%3D&md5=d0d0303cb5416fae3f39b97e8733de8cCAS |
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14.
| Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovV2ltbo%3D&md5=8d51b8728fa1075fdec82573fb56fbbcCAS | 14513379PubMed |
Xue G-P, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R (2008) Molecular dissection of variation in carbohydrate metabolism related to water soluble carbohydrate accumulation in stems of wheat. Journal of Plant Physiology 146, 441–454.
Zadoks JC, Chang TT, Konzak CF (1974) Decimal code for growth stages of cereals. Weed Research 14, 415–421.
| Decimal code for growth stages of cereals.Crossref | GoogleScholarGoogle Scholar |
Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61, 1959–1968.
| Temperature stress and plant sexual reproduction: uncovering the weakest links.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFGjsb8%3D&md5=ce84baf2fe4fd96620635590a97ad30cCAS | 20351019PubMed |