Can elevated CO2 buffer the effects of heat waves on wheat in a dryland cropping system?
Introduction
Atmospheric carbon dioxide concentration [CO2] has rapidly increased from a steady ∼280 μmol mol−1 prior to the Industrial Revolution to currently ∼405 μmol mol−1, and is predicted to reach ∼550 μmol mol−1 by the middle of this century (IPCC, 2014; Pearson and Palmer, 2000). This rise in [CO2] drives an increase in global mean temperatures by 1.0 to 3.7 °C by the end of the 21st century. In addition, heat wave events (short periods of high temperatures) are likely to become more frequent and more severe (IPCC, 2014). Changes in global climate are already adversely affecting yield and quality of important food crops, such as wheat (Triticum aestivum L.), and are predicted to have more severe impacts in future climate scenarios (IPCC, 2014).
Aside from driving climate change, the increase in [CO2] alone affects all plant systems (Ziska, 2008). CO2 enrichment studies, in particular Free Air CO2 Enrichment (FACE) experiments, have shown the following effects of elevated [CO2] (eCO2) on C3 crops such as wheat: Greater net CO2 assimilation rate but lowered stomatal conductivity and photorespiration (Ainsworth and Long, 2005; Kimball et al., 2001; Long et al., 2004); increased leaf and canopy water use efficiency and decreased transpiration (Drake et al., 1997; Leakey et al., 2009; Tausz-Posch et al., 2013a) as well as increases in dry matter accumulation and grain yield, mostly derived through increased fertile tiller numbers and sometimes also through increased single kernel weight (Ainsworth and Long, 2005; Dubey et al., 2015; Tausz-Posch et al., 2015). Elevated CO2 can also lead to an increased accumulation of water-soluble carbohydrates (WSC), such as starch and total non-structural carbohydrates in leaves and, in particular, fructans in the stems (Nie et al., 1995; Sild et al., 1999; Smart et al., 1994). In contrast, the concentration of mineral nutrients, particularly of nitrogen (N), is universally reduced under eCO2 in vegetative and reproductive plant parts, translating directly to lower protein concentrations in vegetative tissues and grains, adversely affecting the nutritional and economic value of crops (Cotrufo et al., 1998; Taub and Wang, 2008).
With optimum growing temperatures between 17 and 23 °C (Shanmugam et al., 2013), wheat is very sensitive to heat (Farooq et al., 2011; Slafer and Rawson, 1995). Heat stress occurs when a plant is exposed to temperatures above an upper threshold for long enough to cause irreversible damage (Wahid et al., 2007). For wheat, threshold temperatures impacting growth and yield, are most commonly given between 31–35 °C (Barnabas et al., 2008; Ferris et al., 1998; Fischer, 2011), although some studies have reported high temperature impacts already above a threshold as low as 26 °C (Stone and Nicolas, 1994).
Heat stress decreases net CO2 assimilation rates resulting in decreased photo-assimilate production as well as reduced dry-matter accumulation and yield (Bergkamp et al., 2018; Narayanan et al., 2015; Tahir and Nakata, 2005). When photosynthesis is constrained by heat stress, carbon (C) reserves, such as stem WSC (fructans) in wheat, can be used to fill the grains (Dreccer et al., 2013; Fokar et al., 1998). For example, the contribution of remobilised stem WSC to grain weight can increase from 10 to 20% under non-stress conditions to 30–50% under stress conditions (van Herwaarden et al., 2003; Wang et al., 2012). Similar trends were shown by Zamani et al. (2014) and Tahir and Nakata (2005) who reported that high temperature stress was correlated with increased WSC remobilisation from the mainstem into grains. Nevertheless, grain size and quality are affected by heat stress, with starch deposition into the grain being generally reduced under heat stress resulting in smaller kernels and more N per unit of starch (Stone and Nicolas, 1994; Farooq et al., 2011). Heat stress also induces phenological responses such as accelerated development, thus shortening the duration for the critical grain-filling period (Bergkamp et al., 2018; Stone and Nicolas, 1996).
The timing of heat stress during plant development is important because certain damage mechanisms only apply during particularly sensitive growth stages (Wollenweber et al., 2003). For example, in wheat heat stress shortly before or at anthesis will decrease grain numbers through floret abortion (Fischer, 1985), while stress episodes during the grain-filling stage will decrease grain weight by interfering with carbohydrate supply and translocation into the grains (Telfer et al., 2013).
Most previous research has focused on eCO2 or heat stress separately, and those studies that investigated eCO2 in combination with higher temperature commonly used moderate, continuous warming, not exceeding heat stress thresholds (e.g. de Oliveira et al., 2015). Little is known about the effects of heat waves, short periods of high temperatures, during critical developmental stages, in combination with eCO2, despite the potential of eCO2 to mitigate or interact with heat stress. For example, Shanmugam et al. (2013) reported that heat stress decreased net CO2 assimilation rates in wheat, but when heat-stressed crops were grown under eCO2, assimilation rates remained higher. Also, greater WSC pools under eCO2 (Sild et al., 1999; Smart et al., 1994; Winzeler et al., 1990) may provide greater reserves for C remobilisation into grains, thereby ameliorating the negative effects of heat stress on grain weights.
The present study investigated whether growth under eCO2 protects wheat from effects of heat waves in a dryland cropping system. Immediate and long-term responses to heat waves were recorded from pre-anthesis to maturity, and the experiment was replicated over two seasons. To account for different sensitive growth stages (Wollenweber et al., 2003), separate heat wave treatments were applied pre-anthesis (HT1) and during the grain-filling period (post-anthesis, HT2 and HT3). The experiment was conducted under ambient [CO2] (∼390 ppm, aCO2) and eCO2 (∼550 ppm) at the Australian Grains Free Air CO2 Enrichment (AGFACE) facility in Horsham, Victoria. This location is part of the semi-arid cropping region of the south-eastern Australian wheat belt, representative of globally important water-limited dryland wheat cropping areas, which are at particular risk from increased incidence and severity of climate change driven heat stress events (Sadras and Dreccer, 2015). Heat waves were simulated with mobile heat chambers (Nuttall et al., 2012), and treatment effects on grain yield assessed. Physiological (gas exchange and leaf chlorophyll) measurements were conducted in conjunction with assessments of stem WSC and leaf N concentrations from pre-anthesis through the grain-filling period and related to grain yield and grain N. These investigations were done on mainstems, because of their stable and relatively high contribution to grain yield as opposed to late-forming tillers which are affected by depleting photoassimilate supply (Darwinkel, 1978; Gan and Stobbe, 1995), even without environmental stresses.
In this study, we critically assess whether eCO2 has the potential to ameliorate heat stress effects in wheat when grown in water-limited dryland wheat cropping systems. We determine if eCO2-induced increases in net CO2 assimilation will lead to a greater WSC pool in stems and, if yes, this helps to ameliorate the negative effects of heat stress on grain weights. Add-on effects for grain N are also investigated. In detail, we tested the following hypotheses:
- 1)
Crops grown under eCO2 have greater net assimilation rates than crops grown under aCO2, both pre- and post-anthesis. Heat waves decrease net assimilation rates in crops grown under aCO2, but eCO2 buffers heat wave effects by maintaining net assimilation rates.
- 2)
Increased net assimilation rates in crops grown under eCO2 result in greater stem WSC concentrations. A greater pool of C reserves (WSC concentration) allows greater remobilisation to grains and this results in the maintenance of greater grain yield of eCO2 grown crops subjected to heat waves.
- 3)
Any reduction in grain N under eCO2 is less in crops subjected to heat waves, because grains of heat stressed crops commonly have less carbohydrates relative to nitrogen.
Section snippets
Site description
This experiment was conducted within the AGFACE facility during the 2013 and 2014 growing seasons. The research site of 7.5 ha is located 7 km west of Horsham, Victoria, Australia (36°45ʹ07ʺS latitude, 142°06ʹ52ʺE longitude, 128 m elevation); a semi-arid region of the Australian wheat belt. The average annual rainfall for the site is 435 mm with growing season (June-November) rainfall averaging 274 mm. The long term mean temperature is 16.5 °C. The soil type is classified as a Vertosol under
CO2, weather and phenology
The average seasonal daytime CO2 concentrations achieved in 2013 was 545 ± 42 ppm (mean ± SD) for eCO2 and 393 ± 16 ppm for aCO2 treatment. In 2014, seasonal daytime CO2 concentrations averaged 551 ± 55 ppm for eCO2 and 393 ± 26 ppm for aCO2.
In 2013 and in 2014, the experimental field site received 324 and 115 mm of rainfall during the wheat growing season, respectively, compared to the long term in-growing season average of 274 mm. Rainfall was extremely low in 2014 to the extent that many
Discussion
In this study, the use of the AGFACE facility and purpose-built static heat chambers simulated environments likely to be encountered by wheat crops in semi-arid cropping regions under projected future climate. The experiment was conducted over two contrasting seasons. In 2013, an above-average rainfall year, a longer grain-filling duration provided sufficient time for greater grain yield combined with lower grain N concentration. In contrast, in 2014, a low-yielding season with generally higher
Conclusion
From this study on wheat grown in a dryland cropping system there is some evidence for a general buffering effect of eCO2 against (experimentally imposed) heatwaves. However, results strongly depended on timing of heatwaves as well as environmental conditions during the growing season. An apparent buffering effect of growth under eCO2 against heatwave impacts was found for instantaneous net CO2 assimilation rates in direct response to a pre-anthesis heatwave, when eCO2 grown crops had high
Acknowledgements
The Australian Grains Free Air CO2 Enrichment (AGFACE) program is jointly run by The University of Melbourne and Agriculture Victoria Research with funding from the Grains Research and Development Corporation and the Australian Commonwealth Department of Agriculture and Water Resources. The authors gratefully acknowledge Mahabubur Mollah (Agriculture Victoria Research) for running the CO2 enrichment technology and Russel Argall (Agriculture Victoria Research) and the field team for agronomic
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