The mechanisms of carbon starvation: how, when, or does it even occur at all?

Abstract

Recent observations of increasing vegetation mortality events appear to be a result of changing climate, in particular, an increase in the frequency, length and intensity of droughts (e.g. Allen et al., 2010). The threat of widespread increases in future mortality has rekindled interest in the mechanisms of plant mortality and survival because we do not yet understand them well enough to confidently model future vegetation dynamics (Sitch et al., 2008). In this issue of New Phytologist, Sala et al. (pp. 274–281) provide a viewpoint on the 'carbon (C) starvation hypothesis' (McDowell et al., 2008). Their viewpoint is invaluable for stimulating our field to explicitly refine our definitions and identify the key experiments needed to understand mechanisms of vegetation survival and mortality. Two important conclusions of their paper were that mortality can occur at nonzero carbohydrate levels and that careful experiments focused on the explicit mechanisms of C starvation, as well as on partitioning the roles of hydraulic failure and C starvation, are needed to understand the physiological underpinnings of how plants die. We applaud these conclusions, and agree that hasty acceptance of any hypothesis before adequate testing is foolish. In this commentary, we highlight some of the valuable ideas from Sala et al. and provide additional comments that we hope will prompt careful future tests on the mechanisms of plant mortality. 'The paucity of studies that quantified mortality forces scientists to use data from nonmortality studies to develop hypotheses … we do this at the risk of confusing stress responses with mortality mechanisms.' When the C-starvation hypothesis was proposed (McDowell et al., 2008), it represented an attempt to summarize and interpret the existing literature on vegetation mortality, of which there was a wealth of indirect studies, but a paucity of true, mechanistic tests. The original formulation of the hypothesis suggested that stomatal closure minimizes hydraulic failure during drought, causing photosynthetic C uptake to decline to low levels, thereby promoting carbon starvation as carbohydrate demand continues for maintenance of metabolism and defense. The plant either starves outright, or succumbs to attack by insects or pathogens, whichever occurs first. By contrast, failure to maintain xylem water tension lower than its cavitation threshold results in embolisms, which, if unrepaired, can eventually lead to widespread hydraulic failure, desiccation and mortality. We hoped that the C-starvation and hydraulic failure hypotheses would generate discussion and new ideas; and indeed, as summarized by Sala et al., active discussion is taking place. A primary conclusion from the discussion is that we need clarification of the various mechanisms by which C starvation can occur, if it occurs at all. Plants maintain metabolism through respiratory processes that consume carbohydrates, and in doing so their C budgets must obey the law of conservation of energy, that is, respiration (mols per plant) = photosynthesis + carbohydrate storage − growth. Therefore, if not all carbohydrates are available for metabolism during drought, this will accelerate C starvation by reducing the storage pool available for respiratory metabolism. The current evidence is mixed regarding metabolic limitations to utilize carbohydrates. We reviewed the four carbohydrate studies cited by Sala et al. that included plant mortality, as opposed to publications in which seasonal carbohydrate analyses were performed on plants that did not die (representing 4 out of 16 (or 25%) of the studies on carbohydrate cited by Sala et al.), and agree that no clear pattern of carbohydrate content and mortality emerges. Mortality at nonzero carbohydrates could simply be a result of mortality via other mechanisms, such as hydraulic failure. However, mortality at nonzero carbohydrate contents could also be a result of C starvation because of the increased use of sugars for osmotic balance during drought. These sugars may be unavailable for other metabolic maintenance processes (Chaves et al., 2003; Bartels & Sunkar, 2005; N. G. McDowell & J. Amthor, unpublished; Sala et al.). Consistent with this, a classic paper by Marshall & Waring (1985) demonstrated that shaded trees consumed all of their starch pools and subsequently died (J. D. Marshall, pers. comm.), but their sugar pools remained well above zero. Elevated temperatures accelerated depletion of the starch pools and subsequent mortality, consistent with the recent results from Adams et al. (2009). Given the current available evidence, it is quite possible that not all carbohydrates can be utilized, particularly during drought. The paucity of studies that have quantified mortality forces scientists to use data from nonmortality studies to develop hypotheses (i.e. McDowell et al., 2008; Sala et al.); however, we do this at the risk of confusing stress responses with mortality mechanisms. Parti