Increased carbon uptake under elevated CO₂ concentration enhances water-use efficiency of C4 broomcorn millet under drought

Highlights

• Elevated CO₂ concentration (E[CO₂]) stimulated photosynthesis of broomcorn millet.

• E[CO₂] improved water-use efficiency of broomcorn millet, especially under drought.

• E[CO₂] did not improve antioxidative defense capacity of broomcorn millet.

Abstract

Broomcorn millet (Panicum miliaceum L.) has been cultivated in arid or semi-arid area due to its high drought tolerance. Yet information on how elevated atmospheric CO₂ concentration ([CO₂]) affects the responses to drought of the productivity, photosynthesis, water-use efficiency and drought tolerance of broomcorn millet is lacking. We investigated the effects of elevated [CO₂] and drought on gas exchange parameters, water-use efficiency, physiological indices related to drought tolerance, leaf area and aboveground biomass of broomcorn millet using an open-top chamber experimental facility in North China in 2015 and 2016. Broomcorn millet was grown in pots with or without drought stress under ambient or elevated [CO₂]. Elevated [CO₂] could compensate the negative effect of drought on the leaf area and aboveground biomass of broomcorn millet. This was attributed to the direct stimulation in photosynthesis due to increased carbon uptake under elevated [CO₂]. Elevated [CO₂] significantly enhanced the water-use efficiency of broomcorn millet at both leaf and plant levels, especially under drought condition. Elevated [CO₂] did not significantly affect evapotranspiration, but increased water-use efficiency at the plant level by 15% (2015) and 35% (2016) of broomcorn millet under drought. Elevated [CO₂] did not significantly affect PSII efficiency, antioxidative defense capacity (peroxidase, malondialdehyde) or osmotic adjustment (soluble sugar content and proline). We conclude that elevated [CO₂] -induced increase in carbon uptake and water-use efficiency would increase the productivity of broomcorn millet in semi-arid areas under future high-CO₂ climate.

Introduction

Atmospheric CO₂ concentration ([CO₂]) is predicted to double by the end of the 21st century, which might be accompanied by shifting precipitation patterns and increasing extreme precipitation events (i.e. drought) (Ghannoum, 2009, IPCC, 2013). Elevated [CO₂] has been widely shown to compensate the drought-induced negative impact on growth and yield of C4 species (Leakey et al., 2009, Joseph and Leon, 2009, Allen et al., 2011, Xu et al., 2013, Zinta et al., 2014, van der Kooi et al., 2016). This compensation effect has been attributed to changes in the primary physiological and biochemical processes of CO₂ uptake (Poorter et al., 1996, Long, 1999), but which is relatively less well understood for C4 species.

The C4 species possess a distinct pathway of photosynthesis from C3 species, through which low atmospheric [CO₂] could be concentrated to enable more efficient carboxylation reaction (Ameye et al., 2012, Liu et al., 2013, Naudts et al., 2013, Li et al., 2013). Drought causes inhibition of C4 photosynthesis due to stomatal limitation, i.e. CO₂ limitation on photosynthetic activity, and/or non-stomatal limitation, i.e. reduced activity of enzymes involved in the CO₂ fixation and electron transport, defense and acclimation pathways, as well as changes in leaf anatomy and ultrastructure (Xu et al., 2006, Naudts et al., 2014, Zinta et al., 2014). Elevated [CO₂] has been shown to stimulate photosynthesis and mitigate drought-induced negative effect on photosynthesis for some C4 species (e.g. maize, sorghum and sugarcane) only under mild but not severe drought stress (Gray et al., 2016). Some studies attributed this to the direct effects of elevated [CO₂] on photosynthesis, which is closely related to the intercellular [CO₂] below the saturation point of A/C_i curve, bundle sheath leakiness and immature C4 leaves (Conley et al., 2001, Allen et al., 2011). However, more studies concluded that elevated [CO₂] might alleviate the negative impact of drought on photosynthesis of C4 species predominantly through the indirect effects on leaf water potential or non-stomatal factors due to soil water conservation (Wall et al., 2001, Ainsworth and Long, 2005, Leakey et al., 2006, Leakey et al., 2009, Joseph and Leon, 2009, Morgan et al., 2011, Li et al., 2019).

An abrupt saturation at a relatively low intercellular [CO₂] might confer C4 species some advantages relative to C3 species, in particular higher WUE (Osmond et al., 1982, Long, 1999). Under elevated [CO₂], C4 species use water more efficiently through enhanced photosynthesis and/or reduced transpiration according to the theory of optimal stomatal behavior, especially under drought (Barton et al., 2012). It has been shown that elevated [CO₂] could improve water-use efficiency of maize and sorghum grown under water stress due to a direct or indirect stimulation in photosynthesis (Wall et al., 2001, Allen et al., 2011). Other studies reported that the enhanced water-use efficiency of C4 species grown under elevated [CO₂] was mainly determined by the reduction in crop water use due to reduced stomatal conductance and transpiration (Conley et al., 2001, Chun et al., 2011).

Apart from improving water-use efficiency, C4 species also develop other adaptive strategies to cope with drought stress , including alteration in antioxidative defense metabolism against reactive oxygen species and osmotic adjustment (Razavi et al., 2008, Rosa et al., 2009, Hatata et al., 2013, Zinta et al., 2014, Naudts et al., 2014). Elevated [CO₂] might alleviate the need for antioxidative defense and osmotic adjustment against drought (Tausz-Posch et al., 2013), leading to high drought tolerance in crops (Zinta et al., 2014). These drought-mitigating effects of elevated [CO₂] are important for crops growth under drought condition. However, the underlying mechanisms remain unclear, especially for C4 species.

Broomcorn millet is a C4 plant with a short growth period of 6–12 weeks, high tolerance to low nitrogen and drought, and high water-use efficiency (Han et al., 2019, Liu et al., 2020, Gong et al., 2020). It has been shown that elevated [CO₂] enhances photosynthesis, growth and yield of C4 broomcorn millet under well-watered condition (Morgan et al., 2011; Hao et al., 2017). However, we know little about how elevated [CO₂] would influence the responses to drought of the productivity, photosynthesis, water-use efficiency and drought tolerance of broomcorn millet. We hypothesized that elevated [CO₂] would (1) mitigate the adverse effect of drought on photosynthesis and growth, (2) enhance water-use efficiency, especially under drought, and (3) improve drought tolerance by changing defense and acclimation pathways, including alteration in PSII efficiency, antioxidant defense and membrane fluidity, for broomcorn millet. These hypotheses were investigated by quantifying the responses of photosynthesis, water-use efficiency at the leaf and plant levels, leaf area, biomass accumulation to drought and elevated [CO₂], and identifying relationship of drought tolerance with physiological traits such as fluorescence content, PSII efficiency, peroxidase (POD), malondialdehyde (MDA), soluble sugar content under elevated [CO₂]. This information will help guide water management or breeding through improving the understanding of the mechanisms toward the drought response to elevated [CO₂] for broomcorn millet under future climate.