Historical Perspective

The study of plant physiological responses to the environment (i.e., ‘ecophysiology’) has attracted researchers since early times, starting from Hales’ proposal that plants took their nourishment from the surrounding air (Hales, 1727), through Charles Darwin’s observations on leaf and chloroplast movements in response to external conditions and experimental manipulations (Darwin, 1881a,b; 1882), to Darwin’s son Francis’ early works on the relationship between transpiration and stomatal aperture (Darwin and Pertz, 1911; Darwin, 1916). From its very early re-foundations in modern times, plant ecophysiology has focused on photosynthesis – and transpiration, its undissociable process in terrestrial environments – as the most central physiological characteristic of plants changing in response to the environment. In parallel, considerable progress in the structural and biochemical basis of photosynthesis enabled improvement in the understanding of photosynthetic processes (Calvin and Benson, 1948), the integration of photosynthesis with transpiration and respiration and the view of photosynthesis as the basis for quantitative models of plant growth and crop production. Monsi and Saeki (1953) developed a theoretical frame to describe the distribution of light within plant communities, as Gaastra (1959) worked on photosynthesis in terms of gas exchange along a series of resistances in and out of leaves. Studies on leaf energy balance were initiated (Raschke, 1956; Gates, 1962) and later developed (Monteith, 1973), when portable infrared (IR) gas analysers for measuring photosynthesis became available (Bosian, 1960), allowing field campaigns of measuring photosynthesis in natural environments around the globe (Tranquilini, 1957; Lange et al., 1969; Björkman et al., 1972; Billings, 1973). In the late sixties and early seventies, the C4 pathway was discovered (Hatch and Slack, 1966) as well as the oxygenase activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) (Ogren and Bowes, 1971), revealing a greater diversity of photosynthetic pathways than thought. Meanwhile, photosynthesis-based plant growth models were developed (Brouwer and de Wit, 1969; Penning de Vries et al. 1974). In the late seventies, an optimisation-theory model to explain stomatal behaviour linking photosynthesis to transpiration was developed by Cowan and Farquhar (1977), and the most widely used leaf photosynthesis model was presented (Farquhar et al., 1980a). After those decades, the importance of photosynthesis and related processes (such as transpiration, respiration and growth) was such that, according to several authors, plant ecophysiology in the eighties was fully focused on photosynthesis-related subjects, such as energy and mass exchange (Mooney et al., 1987; DeLucia et al., 2001; see Fig. 1.1).

Historical Overview of Stable Isotopic Studies in Plant Science

Isotopes are atoms of the same element having the same numbers of protons and electrons but a different number of neutrons. Stable isotopes are those that do not decay to other isotopes on the geological timescales, but can themselves be originated from the decay of radioactive isotopes.

The stable isotopes of carbon and oxygen have major relevance for photosynthesis, respiration and photorespiration, and link the carbon and water cycles. Hence, this chapter will attempt to summarise the current knowledge of processes affecting the stable carbon and oxygen isotopic composition of plants and the exchange between plants (and ecosystems) and the atmosphere.

In addition, hydrogen, nitrogen and sulphur isotopes also have major relevance for plant biology and physiological ecology, but these will not be covered here as these subjects are out of the scope of this book.

Early studies and measurements of stable isotopes in plants were initiated by scientists outside biology, with the initial interest developed in physical science and subsequently extended to geology. Studies were focused on deuterium and its variation in nature, as it was the first isotope to be discovered and was the easiest to measure with the equipment then available, mainly spectrographs. It was not until the late 1930s/early 1940s, with the development of a modern sector i eld-isotope mass spectrometer by Alfred Nier ( 1940 ), that precise measurements of other isotopes such as carbon and oxygen became possible.

Preface

Photosynthesis is the physiological process that overwhelmingly supports the Earth’s primary production. For this reason, photosynthesis research has attracted interest worldwide since the earliest foundations of modern science several centuries ago. Renewed interest in photosynthesis research has been spurred in recent decades. In part this is owing to the impressive technological advancements in analysing the molecular and physiological bases of the photosynthetic processes. But interest in photosynthesis also derives from the need to know how global climate change will impact on the primary productivity of the globe, and on ecosystem stability. Being a highly dynamic process, the precise understanding of how photosynthesis responds to environmental changes is crucial to predict how single plants and entire agro- or ecosystems will be affected in a scenario of rising CO2, rising temperature, and large disturbances in water and nutrient cycles. Finally, photosynthesis studies are the cornerstone for the development of new crops better suited for novel purposes, primarily high yield for biomass and biofuel use.

Whereas several books have proficiently addressed the photosynthetic process, the recent important advances in photosynthesis are still in need of comprehensive coverage. To mention just a few: new techniques have been tested for remote sensing of photosynthesis; important limitations of traditional gas-exchange analysis have been highlighted and solutions proposed; advances have been made in the measurements of diffusive resistance of CO2 inside leaves; the mechanistic knowledge of leaf mesophyll conductance to CO2 has been identified as a decisive but often neglected aspect of leaf photosynthetic; an increasing interest has arisen regarding photosynthetic responses to biotic stresses, a field that has been under-explored or totally unrecognised; photosynthetic responses under leaf development and ontogeny have been assessed; evolutionary trends have been described for several photosynthesis-related processes, such as leaf morphology or stomatal responses to environmental cues; and of course, large-scale studies have been performed regarding photosynthesis at ecosystem level, and the response of ecosystems to climate change.

Introduction

The interest of researchers for a more precise estimation of primary productivity of terrestrial ecosystems and its underlying mechanisms dates back to the 1960s, when the International Biological Programme was launched (Lieth and Whittaker, 1975). At that time, primary productivity was assessed almost exclusively by destructive sampling of plant biomass and measurements of growth, whereas gas-exchange measurements were focused on investigating physiological responses and on model parameterisation. Indeed, estimates of photosynthesis and/or respiration of entire plants or ecosystem was limited by technical problems, and measurements performed on single leaves or plant parts were scaled up using knowledge on plant architecture and ecosystem-structure parameters, such as leaf area index or wood area index (Schulze and Koch, 1971; Tenhunen et al., 1990; Pearcy and Sims, 1994; Matteucci et al., 1995). Nevertheless, knowledge on primary productivity of the terrestrial biosphere increased significantly, and the first attempts of regression modelling were performed (Lieth, 1975; Reichle, 1981).

Since then, the interest for scaling physiological processes in time and space has increased strongly (Ehleringer and Field, 1993; Jarvis, 1995) and a series of new technologies have expanded the spatial scale of observations from leaves to canopy, from ecosystems to globe (e.g., Waring and Running, 1998), and the availability of new measurements, such as canopy fluxes through eddy covariance (EC), remote sensing of absorbed radiation and atmospheric CO2 concentration measurements by tall towers, aircraft or high elevation stations, have improved the understanding of biosphere processes at larger and longer scales, providing better constraints to the estimation of photosynthetic fluxes and carbon-budget components by biogeochemical models (Running et al., 1999; Griffith and Jarvis, 2005).

Crop Photosynthesis

Human societies are dependent upon the productivity of domesticated plant species, including cereals, oilseeds, pulse crops, fruits, vegetables and nuts consumed directly by people; also domesticated animals kept for milk, egg and meat production are reared on feed derived from plants, including grains and leguminous and non-leguminous forage species. Thus, the worldwide availability of calories, protein, dietary fats and other nutrients for human sustenance depends directly on the growth, and therefore the photosynthetic activity, of crops. Accordingly, carbon assimilation of crop species has been extensively studied as a matter of practical importance. Most recently, the expanding use of agricultural crops and crop residues as feedstocks for biofuel production has rejuvenated interest in the potential for increased fixation of atmospheric carbon and capture of solar energy by crop species and agronomic systems (Brown et al., 2000; Heaton et al., 2004). All together, the importance of crop productivity has led in recent years to increased efforts for improving crop photosynthesis by means of mutation discovery and/or transgenic (Parry et al., 2009; Mittler and Blumwald, 2010; see Chapter 13) or epigenetic (Hauben et al., 2009; Mittler and Blumwald, 2010) approaches.

The most relevant spatial scale for the study of crop photosynthesis is often the whole-canopy (plant-community) scale. Communities of crop plants are unique in that they tend to be extremely uniform, usually consisting of a single species (indeed, most often a single genotype), with all members closely synchronised in terms of their phenological development. This unusual uniformity greatly simplifies the study and modelling of crop photosynthesis and growth at the community scale, and has allowed the relevant theory to advance very quickly in comparison with other areas of plant ecology. For example, because crop canopies are spatially quite uniform, they can for some purposes be treated as homogeneous surfaces. This allows photosynthesis of crop canopies to be characterised using theoretical approaches similar to those used for single leaves, quantifying such aspects as light absorption and gas exchange in one dimension (i.e., fluxes per unit area, in this case ground area).

Introduction

Whole-plant photosynthesis is a complex process depending on photosynthetic activity of single leaves, plant architecture and plant biomass distribution between support and assimilative tissues. This chapter reviews the importance of whole-plant photosynthesis in ecology and plant science, the possible ways of estimating whole-plant carbon-gain rates and the determinants of whole-tree carbon gain. It further analyses the changes in whole-tree carbon gain in different environments and with plant aging and increasing size. The main message of this chapter is that whole-plant photosynthetic productivity is determined collectively by a series of physiological and structural traits, by within-canopy variation in environmental drivers and by foliage acclimation to the within-plant environmental heterogeneity. Therefore, whole-plant photosynthesis responds differently to the environment than does the sum of single-leaf photosynthetic responses.

Whole-plant photosynthesis: importance for large-scale carbon fluxes

Driven by the need to understand and predict global change, there is strong interest in determinants of vegetation carbon gain at higher scales ranging from whole plants to canopies, landscapes, biomes and globe (e.g., Williams et al., 2004; Ollinger et al., 2008; Duursma et al., 2009). There is a large variation in physiological activity among the leaves of the same plant owing to differences in leaf ontogenetic status, as well as owing to leaf acclimation to within-canopy light, temperature and humidity gradients. Because of this large variation among leaves, the whole-plant performance is difficult to assess from single-leaf measurements (Klingeman et al., 2000), and poor correspondence of single-leaf gas-exchange rates and plant growth has been observed in numerous studies (e.g., Lambers and Poorter, 1992; Lawlor, 1995).