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Drought Induces Opposite Changes in the Concentration of Non-Structural

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Drought Induces Opposite Changes in the Concentration of Non-Structural Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance Frida Piper To cite this version: Frida Piper. Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance. Annals of Forest Science, Springer Nature (since 2011)/EDP Science (until 2010), 2011, 68 (2), pp.415-424. 10.1007/s13595-011-0030-1. hal-00930764 HAL Id: hal-00930764 https://hal.archives-ouvertes.fr/hal-00930764 Submitted on 1 Jan 2011 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Annals of Forest Science (2011) 68:415–424 DOI 10.1007/s13595-011-0030-1 ORIGINAL PAPER Drought induces opposite changes in the concentration of non-structural carbohydrates of two evergreen Nothofagus species of differential drought resistance Frida I. Piper Received: 21 May 2010 /Accepted: 22 July 2010 /Published online: 17 February 2011 # INRA and Springer Science+Business Media B.V. 2011 Abstract • Conclusions Results demonstrate that carbon depletion • Introduction One current explanation for worldwide cannot be predicted from measurements of gas exchange. drought-induced tree mortality states that reduced photo- Drought-induced mobilization of carbon storage appeared synthesis and continued respiration lead to carbon depletion influenced by the drought resistance of the species and by and eventually to carbon starvation. drought intensity. • Methods To determine if variations in gas exchange are consistent with variations in carbon storage, and if such Keywords Carbon starvation hypothesis . Carbon storage . consistency may depend on the drought resistance of a Climate change . Drought . Photosynthesis species, I examined the non-structural carbohydrates (NSC) concentration and gas exchange in seedlings of two Nothofagus species of differential drought resistance under 1 Introduction severe drought—just before death—and under well- watered conditions. Worldwide massive tree mortality is one of the most evident • Results and discussion Drought provoked decreased and concerning effects of drought associated with climate photosynthesis and had no effect on leaf respiration in both change (Adams et al. 2009; Allen et al. 2010; Bréda et al. species, whereas NSC concentrations varied oppositely: it 2006; Liang et al. 2003; van Mantgem et al. 2009). The decreased in the relatively more drought-susceptible species mechanisms involved in drought-induced tree death, howev- (Nothofagus nitida) whilst it increased in the relatively er, remain unclear (McDowell et al. 2008;Salaetal.2010). more drought-resistant species (Nothofagus dombeyi). One appealing explanation that was suggested earlier (Parker Thus, if carbon balance would have been inferred from and Patton 1975) and that emerged again later (Adams et al. gas exchange alone, I would have wrongly concluded that 2009; Bréda et al. 2006;McDowelletal.2008)isthat carbon depletion occurred in both species. In stressed drought produces a decrease in the reserves of carbohydrates seedlings of N. nitida, photosynthesis and NSC concen- (i.e., carbon depletion, Sala et al. 2010)ofplantsand trations were negatively correlated in roots (r2=−0.57, p= eventually mortality. The reasoning behind this explanation 0.03) and not correlated in stems (r2=−0.05, p=0.58), is basically as follows: (1) drought produces stomatal indicating that carbon depletion due to reduced photosyn- limitations on photosynthesis, (2) the level of photoassimi- thesis was not occurring at harvest time, but it took place lates (carbohydrates) decreases, (3) metabolic demand for earlier when water stress was milder. carbohydrates is no longer met by photosynthesis, (4) carbohydrates are mobilized from storage to satisfy a continued metabolic demand, and (5) concentrations of Handling Editor: Erwin Dreyer carbohydrates in storage sites decrease leading to carbon depletion (McDowell et al. 2008). Accordingly, it is * F. I. Piper ( ) proposed that if drought persists the whole-plant carbon Centro de Investigación en Ecosistemas de la Patagonia (CIEP), Bilbao 449 Coyhaique, Chile demand for growth and maintenance becomes progressively e-mail: [email protected] greater than the whole-plant carbon availability (i.e., current 416 F.I. Piper photosynthesis plus storage), resulting in an increasing and Still under well-watered conditions, carbon mobilization ultimately lethal carbon imbalance. Isohydric species are appears to be limited beyond a certain threshold because believed to be more prone to suffer carbon depletion under some levels of carbon are necessary for essential metabolic drought since they avoid low leaf water potentials by closing function in the storage sites (Millard et al. 2007). This their stomata earlier than anisohydric species (McDowell et probably explains why plants fail in the use of carbon al. 2008). The hypothesis of carbon depletion as the reserves as a substitute of current photosynthesis following physiological consequence of drought-limited tree carbon herbivory (Carpenter et al. 2008) or deep shade (Lusk and gain that may trigger tree mortality has not been demon- Piper 2007; Piper et al. 2009). The access of trees to their strated yet, though an increasing number of studies based on own carbon reserves has been found to be even more gas exchange measurements, hydraulic relationships, and/or limited under drought conditions (Carpenter et al. 2008; growth rate have been invoking this explanation (Adams et Ruehr et al. 2009). This means that even if carbon gain has al. 2009; Allen et al. 2010; Liang et al. 2003;McDowellet been strongly reduced by drought and does not match al. 2008;McDowelletal.2009). It may be inappropriate, carbon demands, carbon depletion is not necessarily going however, to conclude that variations in carbon storage are the to occur. In fact, an increase in carbon reserves has been result of only some of the physiological mechanisms that found in many species experiencing seasonal droughts, control the plant carbon balance (e.g., photosynthesis, leaf including isohydric species like pines (Latt et al. 2001; water potential), given that carbon balance is controlled by a Ludovici et al. 2002; Tissue and Wright 1995; Würth et al. complex net of multiple drought-responsive physiological 2005) or under topographically induced drought (Sala and mechanisms (Chapin et al. 1990;Salaetal.2010). An Hoch 2009). As these studies were carried out on tree enhanced comprehension of the effects of drought on plant species that have passed the filters of natural selection for carbon storage seems urgent, as the geographical extent and such drought situations, it is suggested that drought- the intensity of drought are predicted to increase around the induced accumulation of carbon reserves in response to world (IPCC 2007). Direct measurements of carbon storage drought might be more prone to happen in those genotypes on plants that have been affected by drought integrate all the better adapted to drought. Consistently, Regier et al. (2009) physiological mechanisms involved in plant carbon storage, found that the concentration of non-structural carbohydrates and thus, appear to be a more adequate approach to judge if (NSC) increased in a drought-tolerant clone of Populus nigra carbon depletion does occur. submitted to an experimental drought, while the opposite was Since the early study of Parker and Patton (1975), observed in a drought-intolerant clone of the same species. research on drought effects on carbon balance in plants has Thus, the drought resistance of a genotype may be an been focused mainly on the mechanisms constraining important factor in determining whether carbon depletion carbon gain, while the effects of drought on the carbon does occur. demands (i.e., sink activity) have received less attention. I experimentally assessed the effect of a gradual drought The concept of drought-induced carbon depletion emerged on the carbon storage of two isohydric evergreen species of following this tendency, and it was supported by some Nothofagus of differential drought resistance Nothofagus experimental (Guehl et al. 1993) and observational studies dombeyi (Mirb.) Oerst and Nothofagus nitida (Phil.) (Bréda et al. 2006). Sink activity, however, is also limited Krasser by comparing the concentrations of NSC in by drought (Chapin et al. 1990) and hence, carbon seedlings affected and not affected by drought. I also depletion is one of the three possible results of the examined responses of gas exchange and leaf shedding to interaction between whole-plant carbon gain and whole- drought in order to accomplish a more complete interpre- plant carbon demands, where the other two are an increase tation of the mechanisms involved in the variation of in carbon reserves (i.e., carbon accumulation) and no carbon storage. Drought was developed slowly and gradu- carbon storage change (Sala et al. 2010). Some plants, ally to favor conditions inducing carbon depletion and to especially
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