Assessing the mechanisms underlying sunflower grain weight and oil content responses to temperature during grain filling
Introduction
Grain size and composition at harvest are complex traits that show large genotype x environment interactions and result from many processes at both the plant and organ levels. Among environmental factors, temperature and solar radiation during grain filling have been identified as the main drivers of grain weight and composition in several crops such as wheat (Fischer, 1985; Randall and Moss, 1990; Abbate et al., 1997; Daniel and Triboi, 2000), maize (Andrade et al., 2005; Izquierdo et al. 2009), soybean (Zuil et al., 2012; Firas et al., 2020) and sunflower (Aguirrezábal et al., 2003; Izquierdo et al., 2008).
Significant progress has been done on the effect of ISR on grain weight and oil concentration (%) and content (mg grain−1). The individual weight of maize, sunflower and soybean grains decreased when incident solar radiation accumulated during grain filling was reduced (Andrade and Ferreiro, 1996; Andrade et al., 2000). For sunflower, the individual weight and oil concentration of grains exponentially increase up to a maximum with increasing intercepted solar radiation accumulated during grain filling (ISR, Dosio et al., 2000). Moreover, decreasing ISR for a short period during grain filling reduced grain weight and oil concentration (Aguirrezábal et al., 2003). Genetic variability of the response of the weight and oil concentration of sunflower grains to ISR has been reported (Dosio et al., 2000). Part of this variability has been accounted for by the hull type of the hybrid (black and striped hull, Izquierdo et al., 2008).
In contrast to the large body of results in the literature about ISR effects on sunflower grain weight and oil concentration and content, the effects of temperature on these traits are far from clear. Some previous works have investigated the effects of stressing high temperatures on grain weight and oil concentration (Rondanini et al., 2003) but these studies were only focused on the effects of short periods of supra-optimum temperatures (higher than 35 °C) on these traits. Chimenti et al. (2001) found a decreasing curvilinear response of final embryos weight to temperature in semi-controlled conditions. At temperatures higher than 25 °C, there was a reduction in embryo size average of 1.2 % per each °C of temperature increment. This relationship, established for embryos of an inbred line, has not been studied to our knowledge in the whole fruit of other genotypes or sunflower hybrids. It is then unknown whether genetic variability exists for this response as has been proved for many other process (e.g. temperature effects on fatty acids biosynthesis, Izquierdo and Aguirrezábal, 2008).
Studies about the effect of temperature on oil concentration or content are controversial. In experiments performed in the field a positive correlation between mean temperature and oil concentration was observed (Unger and Thompson, 1982; Nagao and Yamazaki, 1984) while in experiments in controlled or semi-controlled conditions, the opposite response has been reported (Harris et al., 1978; Merrien, 1992). Roche et al. (2006) suggested that changes in oil concentration observed in experiments with different sowing dates could be explained by differences in mean temperature during grain filling. While this study deals with three factors simultaneously (sowing date, genotype and water regime) it does not take into account differences in solar radiation intercepted by the plants in different experiments when performing the analysis, despite of the well-known interactions of ISR with the studied factors. Disagreement among reports evidence a high level of complexity in the effect of temperature on sunflower grain yield and composition (Hall, 2004) and points out to the need of deeper studies to elucidate this issue.
Two distinct sets of temperature responses have been proposed to co-exist in the plant for biomass accumulation: i) a short term developmental processes which defines the rate at which the plant cycle progresses, and therefore the duration of the development of organs and ii) a more loosely coordinated step linked to C assimilation via enzyme activities. If the rate of development increases with temperature while photosynthesis does not, this may result in a lower amount of photosynthate accumulated during each phase of the cycle (Parent et al., 2010). In this way, the final effects of temperature on a given trait could be the result of both direct effects on specific metabolic processes (e.g. C assimilation, night respiration, lipid synthesis) and indirect effects trough changes in the rate of development of the plants (e.g. Aguirrezábal et al., 2003).
To identify direct and indirect effects of temperature on grain weight and oil content it is necessary to investigate correlative changes of ISR with temperature. Increasing temperature reduced the grain filling period of sunflower plants (i.e. Villalobos et al., 1996) and the reduction in grain weight produced by high temperature was previously associated to a shorter filling period (Ploschuk and Hall, 1995). Aguirrezábal et al. (2003) showed that ISR during grain filling period determines final grain weight and oil concentration in sunflower, being this effect maximal for ISR accumulated during a period of fixed thermal limits between 250 and 450 °C d af (critical period). Increasing temperature might reduce ISR accumulation during the critical period by shortening the chronological time-length of this window and thus, reduce grain weight and oil content.
Effects of temperature further than those mediated by developmental rate and consequent ISR accumulation (as proposed by Aguirrezábal et al., 2003) would impact on grain weight and oil concentration. For instance, direct effects of temperature on carbohydrates partitioning to maize ears has been observed (Lafitte and Edmeades, 1997). Temperature has been shown to regulate oil synthesis through oxygen availability in Arabidopsis thaliana seeds (Vigeolas et al., 2011). Unfortunately, in sunflower, it is difficult to easily separate the effects of temperature that are mediated by ISR accumulation (indirect effects) from those that are not (direct effects) as compared to other crops (e.g. wheat), due to the absence of visible phenology markers during grain filling, that clearly establish different stages in grain development. Moreover, in natural conditions, incident solar radiation changes are often correlated to temperature variations making both factors difficult to separate. Interactions between the effects of temperature and ISR could probably explain the controversies found for oil concentration response to temperature, both in experiments conducted in the field or in controlled or semi-controlled conditions, where incident radiation (and then ISR) is usually lower than natural solar radiation.
Quantifying the combined effects of temperature and intercepted solar radiation during grain filling on grain weight and oil content would not only describe the effect of temperature on sunflower grain and oil weight but it will provide an important advance in the knowledge of the mechanisms that govern oil yield response to environmental factors during grain filling. The objectives of this work were a) to characterize the responses of grain weight and oil content to mean temperature during grain filling in two traditional sunflower hybrids with different hull (black and striped) and b) to determine whether these responses can be exclusively explained by changes in solar radiation intercepted per plant or any effect of temperature non mediated by ISR (direct effect of temperature) during the grain filling period could also be involved.
Section snippets
Experimental design
Two traditional sunflower hybrids with different kind of hull (stripped or black) were used in order to capture differences in responses to environmental factors accounted by hull type, as described by Izquierdo et al. (2008). The traditional sunflower hybrids ACA885 (striped hull) and DK3820 (black hull) were studied in two kinds of experiments:
Temperature effects on GW and OC in growth chambers experiments
Experiments conducted in growth chambers allowed evaluating temperature effect during grain filling period under controlled conditions, avoiding correlative variation of incident radiation as well as differences among treatments in growth temperature before anthesis. Grain filling duration did not differ between hybrids but it was affected by treatments. Considering calendar days, the grain filling period was shortest (34 days) at the highest MT (24 °C), and it linearly increased with
Discussion
In this work, two experimental approaches have been utilized to assess the responses of sunflower grain weight and oil content to temperature: i) temperature manipulation at constant incident radiation in growth chambers; ii) modification of radiation interception in field experiments in different locations and in different years (different mean temperatures). Under constant and low incident radiation (growth chambers), final grain weight and oil content responded to temperature with a similar
Conclusion
The combination of growth chamber and field experiments observations allowed to unravel different mechanisms underlying the responses of GW and OC to temperature: at low incident radiation, temperature affects GW exclusively by modifying ISR accumulation (indirect effects) while at higher radiation, temperature displays both direct and indirect effects on GW. OC is affected by temperature in both direct and indirect way disregarding radiation intensity. According to results obtained in the
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
This work was supported by the Instituto Nacional de Tecnología Agropecuaria (INTA) PNCER 2345, Agencia Nacional de Promoción Científica y Tecnológica PICT04 20-21445, Consejo Nacional de Investigaciones Científicas y TécnicasPIP6454, Consejo Nacional de Investigaciones Científicas y TécnicasPIP0541, and Universidad Nacional de Mar del Plata (UNMdP). Authors wish to thank Luis Méndez (INTA-EEA Balcarce) for technical assistance
References (46)
- et al.
Grain yield in wheat: effects of radiation during spike growth period
Field Crops Res.
(1997) - et al.
Reproductive growth of maize, sunflower and soybean at different source levels during grain filling
Field Crops Res.
(1996) - et al.
Prediction of sunflower grain oil concentration as a function of variety, crop management and environment using statistical models
Eur. J. Agron.
(2014) - et al.
Embryo-growth rate and duration in sunflower as affected by temperature
Field Crops Res.
(2001) - et al.
Effects of temperature and nitrogen nutrition on the grain composition of winter wheat: effects on gliadin content and composition
J. Cereal Sci.
(2000) - et al.
Night temperature and intercepted solar radiation additively contribute to oleic acid percentage in sunflower oil
Field Crops Res.
(2010) - et al.
Changes in seed yield and oil fatty acid composition of high oleic sunflower (Helianthus annuus L.) hybrids in relation to the sowing date and the water regime
Eur. J. Agron.
(2002) - et al.
Responses to temperature of fruit dry weight, oil concentration, andoil fatty acid composition in olive (Olea europaea L. var. ‘Arauco’)
Eur. J. Agron.
(2014) - et al.
Night temperature affects fatty acid composition in sunflower oil depending on the hybrid and the phenological stage
Field Crops Res.
(2002) - et al.
Sunflower simulation using the EPIC and ALMANAC models
Field Crops Res.
(1992)
Temperature effects on radiation use and biomass partitioning in diverse tropical maize cultivars
Field Crops Res.
Capitulum position in sunflower affects grain temperature and duration of grain filling
Field Crops Res.
Dynamics of fruit growth and oil quality of sunflower (Helianthus annuus L.) exposed to brief intervals of high temperature during grain filling
Field Crops Res.
Responses of sunflower yield and grain quality to alternating day/night high temperature regimes during grain filling: effects of timing, duration and intensity of exposure to stress
Field Crops Res.
Oil quality of maize and soybean genotypes with increased oleic acid percentage as affected by intercepted solar radiation and temperature
Field Crops Res.
Weight per seed and oil concentration in a sunflower hybrid are accounted for by intercepted solar radiation during a definite period of seed filling
Crop Sci.
Autoregressive model fitting for control
Ann. Inst. Stat. Math.
Crecimiento y rendimiento comparados
Physiological determinants of crop growth and yield in maize, sunflower and soybean
J. Crop. Improv.
Biomass allocation in old-field annual species grown in elevated CO2 environments: no evidence for optimal partitioning
Glob. Change Biol.
The effect of temperature on the oil content and fatty acid composition of the oils from several seed crops
Can. J. Bot.
Solar radiation intercepted during seed filling and oil production in two sunflower hybrids
Crop Sci.
Post-flowering assimilate availability regulates oil fatty acid composition in sunflower grains
Crop Sci.
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