Introduction

The evolution of oxygenic photosynthesis played an important role in the oxygenation of the atmosphere of the Earth. This rise in O2 also had an impact on the subsequent evolution of the photosynthetic organisms themselves, enabling them to develop more efficient bioenergetic systems. Thus, the reduction/oxidation (redox) reactions of the PET chain of green algae and higher plants and their regulation have become adapted to the O2-rich atmosphere of the Earth. Oxygen is, however, not only a product of photosynthesis but it is also a regulator of PET-chain activity and photosynthetic metabolism. Molecular O2 (3O2), is highly reactive and thus inherently toxic, but aerobic cells have evolved the ability to harness the energy potential of aerobic metabolism while minimising potentially harmful effects. Partly this is achieved by using the ROS, such as superoxide (O2–), hydrogen peroxide (H2O2) and singlet oxygen (1O2), formed as by-products of photosynthesis as important metabolic signals. The complex interactions of molecular O2 with the cellular electron-transport and metabolic systems of the cell have become an intrinsic feature of plant redox regulation and homeostasis.

Coordination between energy producing and energy utilising processes is at the heart of the processes that regulate photosynthesis and ensure efficient functioning over a wide range of environmental conditions. Respiration works alongside photosynthesis to secure efficient biological energy production in plant cells. However, unlike the regulation of respiration, which is driven by metabolic substrates that are protected from depletion by effective control mechanisms, the driving force for photosynthesis is the free energy of light, a substrate that cannot be conserved except through light harvesting, efficient charge separation and electron transport. The efficiency of the conversion of the free energy of light into chemical free energy by photosynthesis has been optimised during evolution. A complex network of defence systems protects photosynthesis against the potentially harmful effects of excess light, i.e., light capture that is in excess of the amount that can be used to drive photosynthesis. Efficient dissipation mechanisms are available to protect the photosynthetic membranes and their protein and pigment components by releasing the energy absorbed from light, largely as heat. Photosynthesis is thus able to operate in a highly flexible manner, harvesting energy efficiently at low irradiances and dissipating excess energy at high irradiance.

Photosynthesis in the Cold and the Snow?

In this chapter we discuss photosynthesis and productivity of plants in arctic, alpine and boreal environments. These environments are characterised by cold climate and dominated by plants that thrive in these harsh and often not very productive environments. We concentrate on alpine plants from ‘non-tropical’ mountains and on higher plants, reflecting mostly our own experience and the larger body of literature, which is available for the non-tropical mountains, as well as the need to focus on general aspects. It is noteworthy to mention that there is a growing number of fascinating studies on tropical and subtropical mountain ecosystems, such as the Andes or the Tibetean plateau. However, here we aim to focus on the general features of alpine environments. We will not be able to address the vast diversity of microclimatic and local differences occuring thoughout the number of temperate and tropical alpine ecosystems. We will also omit the effects of UV-B radiation on plants, as this important abiotic factor is not exclusive to mountain environments.

Climatic conditions of arctic, boreal and alpine environments challenge photosynthesis of plants in several ways. During the winter, plants are either covered by snow, which creates a relatively sheltered environment, or they are exposed to cold temperatures as well as ice and snow particles blown by wind. These particles might cause mechanical damage by abrasion on leave surfaces of evergreen plants. As Thomas Elliot wrote: ‘April is the cruelest month. Winter kept us warm, covered by the forgetfulness of snow’. Spring does not necessarily mean less-harsh conditions and smaller challenges for photosynthesis. Temperatures are changing rapidly from sub-zero to high temperatures, and irradiance levels can be extremely high, imposing stress and causing photoinhibitory damage to photosynthetic tisssue. At the same time, plants must prepare themselves rapidly for life during a short summer, during which they need to acquire all the carbon required for reproduction as well as growth and respiration through the next winter.

Introduction

Periods of leaf development and senescence comprise a significant fraction of leaf lifespan. Therefore, leaf lifetime carbon gain is importantly modified by the overall duration and time kinetics of these processes (Wilson et al., 2001; Morecroft et al., 2003; Grassi and Magnani, 2005). In addition, significant time-dependent changes occur in leaf function in mature non-senescent leaves owing to continuous accumulation of cell walls and concomitant reductions in mesophyll-diffusion conductance, as well as owing to re-acclimation of foliage to dynamically changing environmental conditions. Such modifications are of particular importance in evergreen species supporting foliage for several growing seasons, but foliage structure and physiological potentials also change in mature non-senescent leaves in deciduous species (Flexas et al., 2001; Wilson et al., 2001; Niinemets et al., 2004a).

A large body of information of fine-scale regulation of leaf development and senescence has become available (Dengler and Kang, 2001; Kessler and Sinha, 2004; Fleming, 2005; Lim et al., 2007). Although these studies cover in depth the regulatory sequences and signalling pathways during leaf development and senescence, the last comprehensive series of reviews on leaf photosynthetic modifications in developing leaves was published in 1985 (Shesták, 1985). Furthermore, the available treatises of leaf ontogenetic effects on photosynthesis have focused on herbaceous plants or on fast-growing deciduous trees. However, the rate of developmental and ageing processes largely differs among species with varying leaf longevity and structure (Miyazawa et al., 2003). Consideration of these functional-type specific variation patterns in leaf development is of major importance for prediction of plant photosynthetic productivity of highly structured natural plant communities consisting of species with varying leaf longevity and architectural constitution.

Introduction

Gas exchange is tightly coupled to evaporation in all living organisms (Woods and Smith, 2010). Photosynthesis of terrestrial plants is associated with water loss because the CO2 needed to be fixed into carbohydrates enters the leaf through stomata with the consequent loss of water from the sub-stomatal cavity to the atmosphere. Leaf-to-air water-vapour gradient is about 100 times larger than the CO2 gradient. Consequently, plants have to tightly regulate stomatal opening in order to avoid leaf dehydration. This causes a wide variation of the ratio between the rate of CO2 uptake (photosynthesis) and the rate of water-vapour loss (transpiration). This ratio expresses the efficiency of the carbon gain with respect to water loss, i.e., water-use efficiency (WUE).

Plant growth and biomass production are thus largely conditioned by the water resources, which are extremely variable in time and space around the globe, therefore water availability along the growing season is a determinant factor for plant-biome distribution and GPP. In general, it is widely established that ecosystem or crop production is closely dependent on soil-water availability (Beer et al., 2007).

Figure 33.1 shows a list of the main biological determinants, related with plant photosynthesis and transpiration characteristics, as well as the main environmental conditions that determine the specific values of WUE and its wide range of variation.

Optical methods

Light absorbed by chl. antenna is converted almost instantaneously into charge pairs in photochemical centres, which makes possible excitation by short flashes or modulated light thus generating various absorption, fluorescence or luminescence responses. The possibility of manipulating light excitation at will, together with the abundance of chromophores in the photosynthetic machinery, has favoured the development of optical monitoring of photosynthesis in vivo. The three complementary dimensions of optical methods, spectral, kinetic and imaging, provide unique tools to investigate the photosynthetic energy metabolism and, beyond, the bioenergetic status of the whole cell.

There is not a one-to-one correspondence between the measuring opportunities offered by various chromophores embedded in the thylakoid membranes and the aspects of the photosynthetic process they allow monitoring (Table 10.1). Starting from the mechanisms of light interactions with pigments, we will introduce the optical methods that have proved useful for studying leaf photosynthesis, using ‘intensive’ parameters (ratios such as Fv/Fm, kinetic amplitudes and time constants) that automatically compensate for variations of signal intensity between leaf samples. Other non-photosynthetic optical methods that can be used simultaneously (blue-green fluorescence (BGF), IR reflectance) will be briefly mentioned. Applications of leaf reflectance and fluorescence to remote sensing will be addressed in more detail in Chapter 15 and light absorption by leaves and canopies in Chapter 16.

Introduction

The photochemical and biochemical processes that utilise solar energy for the synthesis of complex organic molecules have been on Earth for more than 3.5 billion years (Blankenship, 1992). The original photosynthetic mechanisms are thought to have been similar to those of contemporary cyanobacteria, with an oxygen-evolving photosystem that was responsible for the oxygenation of our early atmosphere, although physical processes have also been suggested (Kump, 2008). Evidence of the ancient origins of photosynthesis is seen in the fossil records of stromatolites of Western Australia (Awramik, 1992). Molecular studies show that it is increasingly more likely that photosynthesis evolved after chemolithotrophy (Xiong and Bauer, 2002). The evolutionary path of type-I and type-II reaction-centre systems remains unresolved and there is some debate on whether the earliest O2-producing cyanobacteria used water or bicarbonate as the terminal reductant that led to an aerobic atmosphere (Dismukes et al., 2001). There is evidence that the reaction giving rise to molecular oxygen, and responsible for our contemporary aerobic atmosphere, arose only once and the structural characteristics of its catalytic centre and its mechanism have been conserved ever since (Barber, 2008a,b). The origin of this oxygenic photosynthesis is under debate, with some authors suggesting an origin as early as 3.8 GA (Buick, 2008).

The Calvin-Benson or C3 cycle of carbon reduction evolved early in the history of life and this is reflected in its universal presence in photosynthetic plants. Evolution of the carbon-reducing steps of the Calvin cycle is thought to have occurred when the Earth’s atmosphere was hypoxic and rich in CO2, which may account for the extreme sensitivity of Rubisco, the enzyme responsible for CO2 entry into the Calvin cycle, to contemporary oxygen levels (Ogren, 1984). Presumably, a long period of evolution in a hypoxic atmosphere resulted in a complex pathway of tightly coupled reactions that have not been amenable to evolutionary modification in a way that reduces O2 inhibition of photosynthesis while retaining the original carbon-fixation function. Under current atmospheric conditions, the O2 inhibition of photosynthesis occurs through oxygenation of RuBP and subsequent loss of CO2 through the reactions of photorespiration.

Introduction

Drought, salinity and flooding are among the most important abiotic stresses affecting plant growth and survival in large areas of the globe. They affect natural ecosystems, plantations and croplands, therefore posing large problems to nature conservation and to farmers and foresters. Drought is a major concern not only in the arid and semi-arid zones, but is also increasingly affecting temperate regions that are now subjected to occasional severe drought spells (IPCC2007 www.ipcc.ch). Alternatively, the same IPCC report indicates an increased occurrence of heavy precipitation and tropical cyclone activity, leading to more frequent flooding events. Salinity and flooding are often secondary stresses following years of incorrect and unsustainable irrigation practices, leading to increased soil salinity and the rise of phreatic soil-water. Flooding can have catastrophic impacts on the productivity of arable farmland, as most crops are intolerant to excess water (Voesenek et al., 2006). Moreover, drought and salt stresses are commonly accompanied by high temperatures and high irradiances that exacerbate the negative impact of each stress acting in isolation (Mittler, 2006).

The primary effects of drought and salinity are similar, as salinity in the soil reduces osmotic potential, making it harder for roots to extract water (Munns, 2002; Munns and Tester, 2008). On the contrary, under flooding water availability is high but O2 availability for root respiration is restricted owing to its slow diffusion in water, limiting root growth (Blom and Voesenek, 1996; Bailey Serres and Voesenek, 2008).

Crassulacean-Acid Metabolism is a Specific Mode of Photosynthesis

Essentially a loop of CO2 flow via organic acids, mainly malate, is switched before assimilation of CO2 in the Calvin cycle of C3 photosynthesis (see Chapter 2). This allows fixation of CO2 during darkness in the night. The nocturnally fixed CO2 is transiently stored in the form of organic acids in the cell-sap vacuole. It is remobilised again during the day and assimilated in the light (Fig. 6.1). In the evolution of vascular plants CAM has arisen polyphyletically, i.e., independently many times. In all the branches of the evolutionary tree of vascular plants, beginning with the pteridophyta, we find taxa performing CAM (Fig. 6.2). Polyphyletic evolution of CAM not only occurred between higher taxa such as subclasses and families (Fig. 6.2), but also within families and subfamilies and even within genera, e.g., in the bromeliads (Smith, 1989; Crayn et al., 2000, 2004), the Clusiaceae (Holtum et al., 2004; Gustafsson et al., 2007) and the orchids (Silvera et al., 2009), and there were also evolutionary reversions from CAM back to C3 photosynthesis. CAM emerges as a good example of Darwinian evolutionary adaptive radiation. It must have been a rather simple step to evolve performance of CAM. In fact, there are basically no new metabolic requirements for CAM as compared with the phylogenetically older general metabolism and C3 photosynthesis.

Chilling and freezing temperatures

Low temperatures represent a major abiotic constraint to the distribution, development and productivity of many plant species. Plants have evolved adaptations to cope with chilling or freezing and to be able to acclimate to low temperature (Allen and Ort 2001; Wisniewski et al., 2003; Slot et al., 2005; Ruelland et al., 2009). These include dormancy, rapid acclimation and maintenance of cold hardiness during prolonged low-temperature or freezing periods (Howe et al., 2003; Wisniewski et al., 2003). The responses to chilling differ from the responses to freezing temperatures. In temperate regions, chilling refers to non-freezing temperatures (0–12°C) during the growing season with the lowest temperatures typically occurring during the night (Allen and Ort, 2001). In contrast, freezing or frost requires temperatures below 0°C. Adaptation to freezing includes mechanisms to prevent freezing injuries from the formation of ice inside the plant cell, which would result in deleterious damage or death of the cell (for recent reviews on acclimation to freezing temperatures see Kalberer et al., 2006; Thomashow, 1999; Xin and Browse, 2000). Other mechanisms involved in this process include e.g., changes in lipid composition or the reactive-oxygen-scavenging-system. Together this suite of acclimation responses involving various metabolic, physiological and developmental aspects is called cold hardening or cold acclimation (Xin and Browse, 2000).

The ability of a species to acclimate to low temperatures via the cold hardening process allows one to distinguish cold-hardy from non-hardy plants, e.g., plants that have the genetic capacity to acclimate to chilling or freezing versus plants lacking this genetic information (Allen and Ort, 2001). These cold-hardy plants are typically from cold or temperate environments. Importantly, even cold-tolerant plants are at risk of being killed by low temperatures. For example, unhardened wheat plants, which are genetically adapted to sustain freezing temperatures, will not be able to survive temperatures of –5°C if they are not acclimated to low temperatures through an adequate cold-hardening period (Thomashow, 1999).

Introduction

Arid and semi-arid environments currently cover a third of terrestrial Earth surface. By definition, ‘semi-arid’ refers to environments where insufficient water is available for vegetation growth. Semi-arid regions are characterised by being intermediates between desert (arid) and humid climates (Fig. 29.1), with an annual precipitation (250–1000 mm year–1) typically lower than the potential evapotranspiration (PET). Furthermore, precipitation is concentrated in specific periods of the year, inducing interruptions of the growing season when water availability reaches the threshold that dramatically limits ecosystem functioning. In addition to pronounced seasonality, a third component is the unpredictability of precipitation, resulting in short drought periods even during the humid season. This unpredictability also refers to high year-to-year variability, which increases with decreasing annual precipitation, often leading to alternation of dry and humid cycles lasting several years. The inter-annual variability is also mirrored in actual evapotranspiration (AET).

The availability of precipitation and the topography of the site are the major factors determining the amount of water available for plants. However, a more detailed division of semi-arid biomes should also consider other components of climate. Temperature is a major climatic element differentiating semi-arid ecosystems. Aside from water, low temperatures become a limiting factor for plant productivity and growth in the coolest semi-arid zones, whereas heat stress can limit plant production in savannas and Mediterranean environments. According to Köppen (1936) classical classification, major biomes in semi-arid climates are savannas (Aw according to Köppen), steppes (BS) and Mediterranean-type ecosystems (Cs). Oceanic and tropical influences prevent low temperatures in Mediterranean regions and especially in savannas. Steppes are characterised by continental influences with wide seasonal and daily ranges in temperature.

The Temperate-Forest Environment

The temperate zone is characterised by pronounced seasonality with temperatures of the warmest month generally higher than 10°C and temperatures of the coldest month generally between –10 and 10°C (Köppen, 1936; Russell, 1931). Temperature is arguably the most important climatic variable in temperate forests. Temperatures during warm and cold periods are strongly variable within the temperate-forest biome, depending on continentality, latitude and topography (Fig. 30.1). Total precipitation is generally greater than 50–75 cm year–1 and is more uniformly distributed over the year than in arid (Chapter 28) and in semi-arid (including Mediterranean ecosystems) (Chapter 29) habitats. The annual input of solar radiation is between 2500–6000 MJ m–2, varying with site latitude, cloudiness and topography (Jarvis and Leverenz, 1983).

Temperate forests are dominated by deciduous trees in oceanic and continental areas of the Northern hemisphere, while evergreens dominate in warmer locations and in the Southern hemisphere. In the edges of temperate biome, mixed forest may appear. Thus, on the cold border the transition to steppes is characterised by open conifer or deciduous forests, while there are mixed conifer-deciduous woodlands in the transition to the boreal biome. In the warm border, the transition is characterised by subtropical evergreen forests in humid locations and by the presence of deciduous Mediterranean oaks in more arid sites.

Introduction

One of the most interesting aspects of desert-plant ecophysiology is the complex nature of adaptations that allow them not only to survive but also to reproduce and maintain their populations under the extreme conditions of environmental stress present in these ecosystems. Of course, deserts are defined by having limited rainfall (typically <250 mm annually) and thus produce significant climatic drought stress, but the seasonality of rainfall patterns and thus drought varies across desert regions, as do the plant growth forms that dominate the landscape (Fig. 28.1).

Terrestrial vascular plants, in any environment where water is limiting for growth, face a dilemma. Their uptake of CO2 from the atmosphere can only occur by opening stomata on their exposed organs regulated by guard cells. However, at the same time that stomata are open and CO2 diffuses into green tissues for photosynthesis, water vapour diffuses out of the plant into the surrounding, drier air. A plant’s strategy can be to reduce transpirational loss by keeping its stomata closed and thereby lose no water vapour, but during that time it also fixes no atmospheric CO2 and thus cannot produce new sugars necessary for growth and respiration. Obviously then, stomata must be opened for photosynthesis to occur but at a significant cost to water levels. The hotter and drier the outside air, the more rapid will be the rate of water-vapour loss from plant tissues.