There are two basic leaf types among the vascular plants realm: simple and compound leaves (Givnish, 1979). Whilst in simple leaves a single blade is inserted directly on the petiole, in compound leaves a blade has two or more subunits called leaflets that vary in number, form and connection to the petiole (e.g. palmately compound leaves vs. pinnately compound leaves). Compound leaves has been regarded as more productive than simple leaves due to their lower production cost (Givnish, 1979; Niinemets et al. 1999; Whitfield, 2006; Malhado et al. 2010). With the dissection of the photosynthetic area, compound leaves can maximize foliar area (diluting mass tissue in more projected area) for light capture and hence increase the growth rates (Givnish et al. 1979; Sack et al. 2003; Malhado et al. 2010). Further, the highly dissected venation usually found on compound leaves contributes with the mechanic support through the hydraulic force inside veins avoiding alterations in the leaf mass area (LMA) as occurs in simple leaves (Givnish et al. 1979; Li et al. 2008; Niinemets et al. 2010). For a similar area, compound leaves are more efficient in convective heat exchange, and thus less transpiration is required for cooling (Gates, 1968; Moya & Flexas, 2012; Michaletz et al. 2015). In fact, under identical environmental conditions, the temperature of dissected leaves can be 4°C lower than that of simple leaves (Stokes et al. 2004). Convective heat exchange allows compound leaves to decrease water loss (Gurevitch et al. 1990; Xu et al. 2009), and to tolerate a wider range of temperatures for biochemical reactions to occur such as carbon assimilation (Michaletz et al. 2015). Thus, based on leaf thermoregulation trade-off related to leaf area and transpirational cooling, different responses to drought can be expected between compound and simple leaves (Givnish, 1979; Michaletz et al. 2015).
Compound leaves are on average thinner than simple leaves (Li et al. 2008; de la Riva et al. 2016). Thinner leaves tend to have higher mesophyll conductances (gm), but lower tolerance to drought (Niinemets et al. 2011; Flexas et al. 2014). It has been shown that, when exposed to drought simple leaf species increase LMA by packing mesophyll cells to avoid cellular lysis (Wright et al. 2004; Galmés et al 2007; Xu et al. 2009), whilst compound leaf species do not change LMA (Xu et al. 2009). Thus, whilst in well-watered conditions higher carbon assimilation can be achieved in compound leaves compared to simple leaves, the latter are more drought tolerant (Galmés et al. 2007; Alonso-Forn et al. 2020b).
It is well known that photosynthesis decreases with drought, but whether drought equally affects the two diffusive components of photosynthesis (i.e. stomatal and mesophyll conductance), remains somehow controversial (Grassi et al. 2005; Galle et al. 2009; Ferrio et al. 2012; Nadal et al. 2018a; Alonso-Forn et al. 2020a). While it seems almost universal that plants exposed to drought close stomata to avoid water losses in detriment of carbon assimilation (AN) (Cornic et al. 2000; Nadal et al. 2018b; Alonso-Forn et al. 2020a), for the mesophyll conductance (gm) some studies have shown that gm decreases with drought (e.g. Galle et al. 2009; Cano et al. 2013; Ouyang et al. 2017) whilst others have found no changes (Galmés et al. 2007; Hommel et al. 2014; Ouyang et al. 2017). Further, to what extent leaf-shape related differences in diffusion photosynthetic traits affect carbon assimilation during drought remain elusive.
Mediterranean-type ecosystem are characterized by severe droughts during summer, and they occur only in five regions of the world: California, South Africa, southeast of Australia, the Mediterranean basin, and central Chile (Lawrence, 1987; Arroyo et al. 1995; Mooney et al. 2001; Armesto et al. 2007). Mediterranean plant species exhibit several morpho-physiological traits to deal with drought such as sclerophyllous leaves, low leaf areas, increased efficiency in photosystem II, increases in the water use efficiency, and high RuBisCO specificity (Delfine et al. 2001; Galmés et al. 2005, 2007; Medrano et al. 2009; Galle et al. 2011; Flexas et al. 2014; Alonso-Forn et al. 2020ab). In the Mediterranean-type climate zone of central Chile species with simple and compound leaves coexist (Mooney & Dunn, 1970; Arroyo et al. 1995). Unlike other Mediterranean-type climate zones where some rainfall events usually occur during the growth season, in central Chile plants must cope with long droughts with no rain during months (Parson, 1976; Schultz, 2005). Moreover, central Chile has experienced an uninterrupted sequence of dry years since 2010 with mean rainfall deficits of 20–40% (Garreaud et al. 2020). The so-called Mega Drought (MD) is the longest event on record and with few analogues in the last millennia, with detrimental effects on water availability (Bozkurt et al. 2018), vegetation and forest fires that have scaled into social and economic impacts (CR2 2017). Recently, Miranda et al. (2020) used temporal trends in the Normalized Difference Vegetation Index (NDVI) to show that the extreme drought of 2019 significantly reduced NDVI (browning) in near one-third of the region's forests and that the highest browning was observed in sclerophyllous forest dominated by species that have been catalogued as tolerant to drought. Further, global climate models project that observed climate trends are likely to be preserved and the number of extreme drought events will be increasing during the rest of the 21st century, which may have a detrimental impact on these ecosystems (Matskovsky et al. 2021). Therefore, it is important to understand how different representative species of this ecosystem would be affected in their photosynthesis to future increased episodes of extreme drought as well as to assess the underlying mechanisms.
In the present study, we evaluated the photosynthetic response to an extreme experimental drought in compound and simple leaf species of the Central Chile matorral. We hypothesized that with no water limitation compound leaf species will show a higher AN than simple leaf species associated with a higher CO2 diffusion inside the leaves (gm). Nevertheless, with an extreme drought simple leaf species will be less affected than compound leaf species because of their stress-tolerant physiology, showing fewer changes in their photosynthetic traits.