Mechanisms Linking Drought, Hydraulics, Carbon Metabolism, and Vegetation Mortality

Abstract

Events of regional-scale vegetation mortality appear to be increasing in a variety of biomes throughout the Earth and are frequently associated with increased temperatures, droughts, and often (but not always) with outbreaks of biotic agents such as insects and pathogens (for review, see Allen et al., 2010; Supplemental Information S1). The precise physiological mechanisms underlying plant mortality are poorly understood, which limits prediction of where, when, and how vegetation will change with future climatic variation (for review, see Supplemental Information S2). In particular, hypotheses regarding carbon starvation (failure to maintain metabolism or fend off biotic agents due to prolonged negative carbohydrate balance) and hydraulic failure (desiccation from failed water transport) have stimulated recent debate (Adams et al., 2009a, 2009b; Leuzinger et al., 2009; Sala, 2009; McDowell and Sevanto, 2010; Sala et al., 2010). In this Update, I offer a perspective on the mechanisms of drought-induced mortality by providing an integrated view of carbon metabolism in relation to stress and mortality, linking carbon metabolism with new evidence on the role of hydraulic failure in mortality, and identifying associated uncertainties. Drought is the predominant climate characteristic associated with mortality (Allen et al., 2010), but there are parallels with low temperature, light, and paleo-CO2 concentrations, from which I have cautiously drawn evidence regarding mechanisms of drought-induced mortality. Two novel results emerged from this review. First, well-known carbohydrate partitioning patterns are consistent with observations of carbohydrate concentrations in stressed but surviving plants as well as those that are dying, and these results support carbon starvation as a threat to survival during drought. Second, carbon metabolism and hydraulics are coupled via multiple interactions that are only recently becoming appreciated, including an enhanced risk of mortality in species that maintain narrow margins of hydraulic safety. Starve (v): “…to perish or be in process of perishing from lack or insufficiency of food…” (Oxford English Dictionary, 2009). I define the process of carbon starvation as any situation in which carbon supply from photosynthesis and the mobilization of nonstructural carbohydrates (NSC) and autophagy (vacuolar proteolysis) is less than carbon use by respiration, growth, and defense. Death is defined as thermodynamic equilibrium between the organism and the environment, in which plants no longer have energy gradients to drive metabolism or regenerate. According to these definitions, measurable NSC need not be zero at death, but any remaining NSC must be unavailable to metabolism (i.e. “accessible carbon exhaustion”; Sala et al., 2010). Drought can put plants on the path to carbon starvation, but they may eventually die of another mechanism. Moreover, there are potential interactions between the path to carbon starvation and (1) utilization of energy stores for metabolism and defense; (2) carbohydrate transport processes, including phloem loading, unloading, and transport; and (3) the demand for energy and carbon skeletons needed to maintain turgor and photosynthesis. The importance of these processes (described below), as well as the widespread observations of elevated NSC in plants during periods of stress (Chapin et al., 1990; Körner 2003; for further review, see Supplemental Information S3), has led to recent debate regarding the mechanisms of carbon starvation or whether it even occurs at all. One interpretation of these observations is that the carbon starvation process is unimportant and water stress induces mortality via hydraulic failure, limiting NSC utilization or predisposing plants to lethal attack by biotic agents (McDowell et al., 2008; Sala et al., 2010). I propose an additional interpretation: water stress impacts on hydraulics, NSC transport, and the use of NSC for metabolism and defense accelerate the process of carbon starvation, which feeds back on further starvation for carbon and associated vulnerability to biotic attack. During water stress, plant growth declines before photosynthesis, resulting in a NSC surplus (Luxmoore et al., 1995; Estiarte and Peñuelas, 1999; Kozlowski and Pallardy, 2002; Hummel et al., 2010, Pinheiro and Chaves, 2011). This NSC surplus results because water stress causes greater reductions in growth than photosynthesis (Supplemental Information S4) and greater reductions in photosynthesis than maintenance respiration (Supplemental Information S5). A modeled representation that summarizes these observations is shown in Figure 1 and described in the Supplemental Data (Amthor and McCree 1990). An important result of this simulation is that carbohydrate content increases early in the drought, but if drought causes significantly reduced photosynthesis for a sufficiently long period, then NSC content will eventually decline, as NSC is consumed for t