Carbon and Water Relations in Pinus Taeda: Bridging the Gap across Plant Physiology, Genomics, and Global Climate Change

Abstract

<p>Plants respond to changes in their local environment and, at the same time, influence the environment at a global scale. The molecular and physiological mechanisms regulating this interaction are not completely understood and this limits our capacity to predict the response of vegetation to future environmental changes. This dissertation combined tools from genomics, physiology, and ecology to examine the response of plants to environmental change. Specifically, it focused on processes affecting carbon and water exchange in forest trees because (1) trees are long-lived species that might face repeated environmental challenges; (2) relatively little information exists about the genes and the molecular mechanisms regulating structural and physiological traits in adult, long-lived woody plants; and (3) forest trees exchange a significant amount of carbon and water with the atmosphere and are therefore major players in the global carbon and water cycles. </p><p>Water flux through forests depends both on environmental conditions (e.g., soil moisture) and on the hydraulic architecture of individual trees. Resistance to xylem cavitation is an important hydraulic trait that is often associated with drought tolerance but potentially at the cost of reduced carbon uptake. The second chapter of this dissertation evaluated the variation in resistance to xylem cavitation, hydraulic conductivity, wood anatomy traits, and leaf gas exchange across 14 co-occurring temperate tree species including both angiosperms and gymnosperms. The relationship between vulnerability to cavitation (ψ₅₀) and hydraulic conductivity within specific organs (i.e. stems and roots) was not significant when considering the phylogenetic association between species. However, even after phylogenetic correction, photosynthetic carbon uptake (A) was positively correlated with both stem and root ψ₅₀, and stomatal conductance (g_s) was strongly correlated with root ψ₅₀ . These results suggest that there is a trade-off between vulnerability to cavitation and water transport capacity at the whole-plant level, and that this functional relationship reflects an adaptive response to the environment. </p><p>Forests are an important component of the global carbon cycle that can be directly impacted by a rise in atmospheric CO₂ concentration.. The third chapter of this dissertation investigated the effects of long-term exposure to elevated CO2 on the gene expression of mature, field-grown loblolly pine trees. Using cDNA microarrays, I compared the expression of 1784 pine transcripts in trees growing under ambient and those under elevated CO₂ at monthly intervals throughout a growing season. Overall, more genes were upregulated than downregulated by elevated CO₂, although the total number of genes differentially expressed varied throughout the season. The pattern of increasing number of differentially expressed genes until the peak of the growing season (July and August) followed by a decrease in that number, matched the seasonal trend of tree growth and photosynthetic response to elevated CO₂ in this species. The seasonal trend also reflected the interaction among multiple abiotic factors intrinsic to field conditions and emphasized the relevance of evaluating the role of genes in their natural environment. Genes consistently upregulated by elevated CO₂ were functionally associated with environmental sensing, cellular signaling, and carbon metabolism, in particular the degradation of carbohydrates through respiration. An increase in carbohydrates degradation is particularly relevant in the context of carbon balance of forest trees because of the potential for enhanced leaf and tree respiration leading to a reduced sink capacity for CO₂. </p><p>Loblolly pine produces several flushes of needles throughout the year each with an average lifespan of 19 months. Each year, two age classes of needles contribute to the annual carbon sequestration of the loblolly pine forest. To address the impact of leaf age on the effects of elevated CO₂ in carbon metabolism regulation, I compared the gene expression profiles from trees under ambient and elevated CO₂ conditions in two needle cohorts: one-year-old and current-year. Differential expression under elevated CO₂ was seven times more frequent in current-year than in one-year-old needles. Despite differences in magnitude, many of the patterns within specific groups of genes were similar across age classes. For instance, there was a trend for downregulation of genes involved in the light-reactions of photosynthesis and those in photorespiration in both age classes, while genes associated with dark respiration were largely upregulated by elevated CO₂ in both cases. The difference between the two cohorts was particularly evident in the group of genes related to energy production (ATP synthesis) and the group associated with carbon partitioning (sucrose and starch metabolism). Because sucrose and starch metabolism categories included many genes known to be important regulators of gene expression and plant physiological processes, this suggests that this stage of carbon metabolism might be an important control point in age-dependent foliar responses to elevated CO₂.</p><p>This dissertation examined both structural and physiological components of plant water and carbon relations (Chapter 2) across different biological scales of organization (whole-plant level in Chapter 2; gene-level response to ecosystem-level changes in Chapters 3 and 4) and reflecting adjustments at distinct temporal scales (life-span of the organism vs. evolutionary selection of traits). An integrative approach was used to advance our understanding of how plants acclimate and adapt to their environment, and to provide a mechanistic framework for predictive models of plant response to environmental change. </p>