Assessing the mechanisms underlying sunflower grain weight and oil content responses to temperature during grain filling

Highlights

• Sunflower grain weight and oil content show bilinear response to mean temperature.

• Oil content is more sensitive to temperature than other grain components that contribute to grain weight.

• Mean temperature and intercepted solar radiation exert interactive effects on grain weight.

• Mean temperature and intercepted solar radiation exert additive effects on oil content.

• Different mechanisms underlay the responses of grain weight and oil content to temperature.

Abstract

Temperature and solar radiation during grain filling are the main drivers of grain weight and composition in several crops. While significant progress has been done on the effect of solar radiation intercepted by the plants (ISR) on grain weight (GW, mg) and oil content (OC, mg grain⁻¹) of sunflower (Helianthus Annus L.), the effects of temperature on these traits are far from clear. As temperature affects the rate of plant development, increasing temperature would shorten grain filling duration and so, the critical period for ISR effect on GW and OC (indirect effect of temperature). However, direct effects of temperature non-mediated by ISR accumulation could also affect these traits. 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 and b) to determine whether these responses can be exclusively explained by changes in ISR or any direct effect of temperature should also be considered. Two experimental approaches have been used to address these objectives: i) temperature manipulation at constant incident radiation in growth chambers; ii) modification of radiation interception in the field in different locations and years (different mean temperatures). Growth chamber experiments showed that GW and OC respond to temperature in a plateau lineal shape. At low incident radiation such as that of growth chambers, temperature effects on GW can be exclusively explained by reductions in ISR, while both direct and indirect effects of MT are evident on OC. Results obtained in field experiments confirmed this behavior at low radiation. Both GW and OC exponentially increased up to a maximum with ISR disregarding MT. Mathematical models were established to describe the responses of GW and OC to MT and ISR. These models consider MT x ISR interactive effects on GW; and MT - ISR additive effects on OC. 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 intensity, increasing temperature decreased GW exclusively by reducing ISR accumulation (indirect effects) while at higher radiation, temperature displays both direct (non-mediated by ISR) and indirect (ISR mediated) effects on GW. OC is affected by temperature in both direct and indirect way disregarding ISR. This work constitutes an important contribution towards understanding the effect of temperature during grain filling on sunflower yield and its relationship to solar radiation effects.

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.