Research paperYield, growth and grain nitrogen response to elevated CO2 in six lentil (Lens culinaris) cultivars grown under Free Air CO2 Enrichment (FACE) in a semi-arid environment
Introduction
Atmospheric CO2 concentrations ([CO2]) have been increasing from about 280 ppm to 406 ppm from the pre-industrial era until now (January 2017; www.co2.earth; last accessed 23 February 2017). If global greenhouse gas emissions remain at the 2010 level, then atmospheric CO2 concentrations ([CO2]) should reach 550 ppm by 2050 (IPCC, 2014). This increase in the substrate of photosynthesis has direct implications for plant metabolism, such as increased growth and yield, at least in C3 plants and in the absence of changes in temperature and rainfall patterns (Ainsworth and Long, 2005, Ziska et al., 2012). Elevated [CO2] (e[CO2]) also reduces stomatal conductance, leading to higher transpiration efficiency (Leakey et al., 2009, Tausz-Posch et al., 2013) and potentially increased crop water productivity under conditions of water stress (Deryng et al., 2016, Gifford, 1979). In environments prone to severe terminal drought (where the crop progressively runs out of water with no resupply), there are however concerns that the early increases in leaf area and biomass accumulation under e[CO2] might negate the water savings from higher transpiration efficiency, potentially leading to an earlier onset of drought. This could reduce post-flowering growth and translocation of assimilates and therefore reduce the yield response to e[CO2]. There are few FACE experimental set-ups that directly address this type of water stress, and experimental data to support or disprove this theory is sparse (Deryng et al., 2016).
Higher growth and grain yield are often associated with decreased grain quality, especially in cereals, where decreases in grain nitrogen concentration ([N]) and therefore protein concentrations, raise concerns about nutrition and product quality (Jablonski et al., 2002, Myers et al., 2014). Decreased grain [N] under e[CO2] is preceded by decreases in [N] in vegetative biomass, particularly in leaves (Leakey et al., 2009). There are several hypotheses to explain this decrease in tissue [N] (reviewed by Taub and Wang, 2008). The dilution hypothesis contends that N supply fails to keep up with the increased demand from stimulated biomass growth. Legumes, with their nitrogen-fixing symbionts, would be able to overcome such limitation because the additional carbohydrate acquired under e[CO2] could feed the N-fixing symbiosis (Rogers et al., 2009). Indeed, field grown soybean did not show decreases in leaf [N] from about mid-season onwards, once the N-fixing symbiosis had established (Rogers et al., 2006). Studies in chambers or high rainfall agro-ecosystems suggested that, in contrast to cereals, legume grains maintain protein concentrations under e[CO2] (Jablonski et al., 2002; Taub et al., 2008). As N-fixation is more sensitive to water stress than biomass accumulation and leaf expansion (Serraj et al., 1998), in semi-arid environments N-fixation is likely interrupted by water stress and therefore biomass dilution of [N] might occur. Some recent reports have found small but significant decreases in grain protein in legumes which might be partially explained by water stress (Lam et al., 2012 in chickpea (Cicer arietinum); Bourgault et al., 2016 in field pea (Pisum sativum)).
It might be possible to take advantage of rising atmospheric [CO2] by selecting for greater CO2 responsiveness in crop breeding programs either directly or by selecting traits that are associated with a greater response (Ainsworth et al., 2008, Tausz et al., 2013, Ziska et al., 2012). Intraspecific variability in the response to e[CO2] − a prerequisite for this approach − has been reported in soybean (Glycine max): Bishop et al. (2015) have found consistent differences in grain yield response to e[CO2] among 18 cultivars grown under Free Air CO2 Enrichment (FACE) and suggested this is a heritable trait. They also suggested that high e[CO2] response is related to a greater harvest index and a short stature. Similarly, Bunce (2008) investigated variability in the response to e[CO2] of 4 common bean (Phaseolus vulgaris) cultivars and suggested that greater grain yield response was associated with the ability to produce more pods under e[CO2]. Similarly, Ziska et al. (2001) showed that greater yield response in soybean was related to the ability of some cultivars to increase the seed production on auxiliary branches. In contrast, studies reporting a lack of response to e[CO2] in one cultivar have often related this to limitations in the ability to use the additional carbohydrates. For example, Sicher et al. (2010) found that a dwarf cultivar of soybean did not show yield increases under e[CO2]. Grains of this cultivar were 75% smaller and had lower oil seed content than grains of normal cultivar. Taken together, these studies suggest that the response to e[CO2] might depend on both the capacity of the plant to utilise the additional carbohydrates produced under e[CO2] and the effective translocation of resources to grains later in yield formation.
Lentil (Lens culinaris) is one of the oldest cultivated crops in the world and its production has more than quadrupled since the 1960s reaching a global production of over 5 million tonnes in 2013 (FAOSTAT, 2016). It is well-known as a nutritious grain and forms the basis of many traditional Asian and Middle Eastern recipes (Raghuvanshi and Singh, 2009). In Australia, it is grown as a winter crop under non-irrigated conditions, and therefore frequently subjected to terminal drought conditions. Further, the crop is often exposed to low temperatures during the vegetative stage and high temperature stress by pod filling (Materne and Siddique, 2009). Substantial efforts in breeding lentils in Australia are recent and expanding genetic variability is still seen as a major activity (Siddique et al., 2013). Intraspecific variability in many traits of interest is adequate and could be used in breeding programs (Erskine et al., 2009), although there is little published information on drought tolerance characteristics and no information on potential intraspecific variability in the response to e[CO2] in lentils.
In this study, we grew a range of lentil lines over three seasons in the Australian Grains FACE (AGFACE) facility. AGFACE is located in the south-eastern Australian grain cropping belt, with a typical semi-arid Mediterranean climate, making it a representative site for significant areas of global lentil production (Materne and Siddique, 2009). Therefore, this experimental set-up allowed us to address the following research questions:
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What are the effects of e[CO2] on the growth and grain yield of lentil (Lens culinaris) grown under realistic drought conditions under Free Air CO2 Enrichment (FACE)?
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Does e[CO2] decrease grain [N] in lentil?
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Is there genotypic variability in the response to e[CO2] in lentil cultivars?
Section snippets
Experimental site and growing conditions
The Australian Grains Free Air CO2 Enrichment (AGFACE) facility is located near Horsham, Victoria (36°45′07″S 142°06′52″E, 127 m above sea level). The site is cracking clay soil (Vertosol) with approximately 35% clay content at the surface increasing to 60% at 1.4 m depth. Long term average (based on 1981–2010 period) annual rainfall is 435 mm, with approximately 320 mm falling during the winter growing season (from May to November inclusive). Average maximum and minimum temperatures are 17.6 °C and
Grain yield and yield components
Grain yield increased in response to e[CO2] and there was a wide range of relative responses between years (32, 138, and 18% in 2013, 2014 and 2015 respectively) (Fig. 3A). The absolute CO2 response in grain yield appeared to be constant at approximately 0.5 t ha−1 regardless of yield potential. This increase in yield was associated with an increase in total above-ground biomass measured at maturity (by 32%; Fig. 3B), harvest index (by 16%; Fig. 3C) and in the number of pods per m2 (by 55%; Table
Discussion
Grain yield increases (18, 32 and 138%) reported here with e[CO2] are relatively large compared to previous FACE studies in two years out of three. Other FACE studies with legumes include the SoyFACE experiment (Illinois, USA), where soybean yields increased on average by 15% (Morgan et al., 2005) and from 0 to 22% depending on the cultivar in a different experiment (Bishop et al., 2015). The mini-FACE array at the Chinese Academy of Agricultural Sciences (Changping, China) also investigated
Conclusion
In this study, e[CO2] increased yields by approximately 0.5 t ha−1 (relative increase ranging from 18 to 138%) by increasing both biomass accumulation (by 32%) and the harvest index (by up to 60%). The response of grain yield and harvest index varied with season, with the greatest response in both parameters observed during a terminal drought. Biomass accumulation post-flowering was increased considerably by e[CO2] (a 50% increase), suggesting that the indeterminate growth habit of lentil
Acknowledgements
Research at the Australian Grains Free Air Carbon dioxide Enrichment (AGFACE) facility is jointly run by the Victorian Government and the University of Melbourne and receives substantial additional funding from the Australian Commonwealth Department of Agriculture and Water Resources (DAFWR) and the Grains Research and Development Corporation (GRDC). We wish to acknowledge the crucial contributions of Mahabubur Mollah (AGFACE research engineer) and Russel Argall (senior technical officer) and
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