Understanding the drought physiology of woody plants has become an increasingly important focus of plant science research in recent years, spurred on by concern about the potential for widespread tree mortality in response to drought stress caused by global warming (McDowell et al., 2008; Allen et al., 2010). However, there is one aspect of how woody plants cope with water deficits that has received very little attention: the role of carbon fixation by photosynthetic bark. This process may become especially important for maintaining physiological activity in woody tissues of drought-stressed trees as the supply of photosynthate from leaves dwindles, due to stomatal closure and impaired phloem translocation. In this issue of New Phytologist, Vandegehuchte et al. (pp. 998–1002) bring this process into the spotlight, and provide a compelling argument for why we should take more notice of that often-hidden, green layer of tissue that is ubiquitous beneath the smooth-bark surfaces of woody plants (Scott, 1907; Pfanz et al., 2002; Dima et al., 2006; Rosell et al., 2015).
‘Vandegehuchte et al.provide a compelling argument for why we should take more notice of that often-hidden, green layer of tissue that is ubiquitous beneath the smooth-bark surfaces of woody plants …’
It is helpful to differentiate two different syndromes with respect to photosynthetic activity in woody stems. The less common of these is that in which net photosynthesis occurs; that is, a net uptake of CO2 from the atmosphere. This typically requires the presence of stomata, or in some cases lenticels, in the epidermis of the stem to facilitate the diffusion of CO2 from the atmosphere into the photosynthetic cells in the bark cortex. This type of stem photosynthetic activity can be found, for example, in some desert shrubs and early successional legumes (Ehleringer et al., 1987; Comstock & Ehleringer, 1990; Ávila et al., 2014). The far more common stem photosynthetic syndrome is one in which chlorophyllous cells in the bark cortex refix a portion of the CO2 respired by the underlying tissues or carried into the stem segment by the transpiration stream as it diffuses from inside the stem to the atmosphere. This kind of stem photosynthetic activity likely takes place in all shrub and tree species that have smooth bark surfaces. In some of these species, smooth bark will be found on only the youngest stems, whereas in others (e.g. some Eucalyptus species) smooth bark will be maintained as the stems age and increase in diameter through successive shedding of dead bark layers (Pfanz et al., 2002; Cernusak & Hutley, 2011). Ávila et al. (2014) recently proposed that the former syndrome be referred to as stem net photosynthesis, and the latter as stem recycling photosynthesis. As the term implies for the latter syndrome, the main function is to recycle some portion of the CO2 that builds up inside the stem as a result of respiratory activity in the woody tissues (Fig. 1). In this commentary, we will focus our discussion on the widespread phenomenon of stem recycling photosynthesis.
As Vandegehuchte et al. point out, stem recycling photosynthesis increases whole plant water-use efficiency (WUE). For stem recycling photosynthesis to occur, moist tissues need not be exposed to the drier atmosphere. No stomatal valves are required to link the stem interior to the external air to supply the CO2 substrate for recycling photosynthesis. Rather, it relies upon internally produced CO2, or CO2 that has been transported into the stem section by the transpiration stream (Teskey et al., 2008). In a comparison of the WUE of gross photosynthesis in bark and leaves of Western white pine, WUE was found to be 50 times larger for bark than for leaves (Cernusak & Marshall, 2000).
In a whole-plant context, it is perhaps easiest to think of the impact of recycling photosynthesis on WUE in terms of an increase in carbon-use efficiency. In general, about half the carbon taken up by photosynthesis in a plant will be respired back to the atmosphere. Since WUE can be defined as the net amount of carbon taken up by a plant for a given amount of water loss, a reduction in carbon loss through stem recycling photosynthesis will increase the overall plant WUE.
Stem recycling photosynthesis produces locally available carbohydrates
One of the challenges that woody plants must cope with under drought is that phloem transport from leaves to woody tissues may become compromised (Sala et al., 2010; Sevanto, 2014). Thus, even though carbohydrate resources may continue to be available in the leaves, the plant may struggle to deliver these to woody tissues where they are needed to maintain the hydraulic conductivity and functionality of stem tissues. Stem recycling photosynthesis, however, can produce locally available carbohydrate resources in close proximity to xylem parenchyma cells, where they can be used for maintenance processes, osmotic adjustment, and xylem embolism refilling (Vandegehuchte et al.). Although in its infancy as a research topic, there is evidence to suggest that light exclusion from bark leads to reduced hydraulic function in the underlying sapwood (Schmitz et al., 2012; Bloemen et al., 2013; Gao et al., 2015), suggesting that stem recycling photosynthesis plays an important role in supporting stem hydraulic function.
Stem recycling photosynthesis works under high temperatures
Prolonged drought events are generally accompanied by high temperatures. Stem recycling photosynthesis has an advantage over leaf photosynthesis at these high temperatures in that the CO2 concentration inside the bark is generally very high, even when the stems are illuminated and their photosynthesis is actively absorbing CO2 (Cernusak & Marshall, 2000). This means that the reduction in the specificity of Rubisco that occurs with increasing temperature is not manifest in the photosynthesis rate in the bark to the same extent that it would be in leaves, because the ratio of CO2 to O2 in the bark is relatively high. As a result, it was observed in branches of Western white pine that gross photosynthesis in the bark continued to increase with increasing temperature, even up to 45°C (Cernusak & Marshall, 2000). But, gross photosynthesis does not increase exponentially with temperature in the same fashion as dark respiration; thus, the proportional refixation rate does decline with increasing temperature (Wittmann & Pfanz, 2007). Nevertheless, stem recycling photosynthesis can continue to provide carbon resources under drought conditions, at high temperatures, when leaf photosynthesis is likely to have all but ceased.
Bark that favours stem recycling photosynthesis also reduces water loss
Because stem recycling photosynthesis relies on internally produced CO2, the development of a low-permeability, outer-most bark layer, also referred to as periderm, will serve to increase the overall recycling rate. This is because such a low-permeability layer will help to trap CO2 inside the bark, thereby increasing the bark photosynthesis rate and the proportion of respired CO2 that can be recaptured. Such a low-permeability layer will also have the added benefit under drought conditions that it will slow the loss of water vapour from the bark surface, and thereby slow the desiccation of the woody tissue. This may become especially important under severe conditions of water deficit, when roots are no longer able to absorb water from the soil, leaves have completely closed stomata, and the plant must outlast the drought by isolating itself hydraulically from the environment. Support for the idea of a low permeability periderm contributing both to stem recycling photosynthesis and to reducing water loss from the woody tissue comes again from observations on Western white pine; in that case, there was a negative relationship between the bark conductance to water vapour and the stem recycling photosynthesis rate (Cernusak & Marshall, 2000).
Is there a cost to stem recycling photosynthesis?
In order to maintain stem recycling photosynthesis as woody tissues age, many tree species will seasonally shed a layer of dead bark, revealing beneath a smooth-bark surface that both traps respired CO2 and allows for light penetration (Cernusak et al., 2001; Pfanz et al., 2002; Cernusak & Hutley, 2011). For a given diameter of branch or stem, these species that maintain their smooth bark have thinner bark than rough-barked species that instead retain successive layers of dead bark (Cernusak et al., 2006; Rosell et al., 2014). However, although rough-bark species may have only limited rates of stem recycling photosynthesis, the underlying cambium is better insulated from fire (Vines, 1968), and possibly from pests and pathogens too. Thus, there potentially exists a trade-off between stem protection from fire and the maintenance of bark characteristics that promote high rates of stem recycling photosynthesis (Cernusak & Hutley, 2011; Rosell et al., 2014). Now that Vandegehuchte et al. have brought stem recycling photosynthesis clearly into focus as an important feature in the drought physiology of woody plants, we can begin to formulate and test hypotheses about its ecological and evolutionary significance with respect to drought, fire, and pest and pathogen pressure.
Thanks to Meisha Holloway-Phillips for kindly commenting on a draft of the commentary. The authors would also like to acknowledge funding from an Australian Research Council Discovery Project (DP120102965).