Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny

Abstract

Contents Summary349I.Leaf growth: volume, structures, water and carbon349II.Coupling water and carbon limitations through the Lockhart model?350III.ABA signalling pathway as a hub to coordinate water and carbon relations353IV.Leaf venation: just a two‐way pipe network?354V.Leaf ontogeny orchestrates the actors involved in the control of leaf growth355VI.The growing leaf in a changing world360VII.Conclusion361Acknowledgements362References362 Summary Leaf growth is the central process facilitating energy capture and plant performance. This is also one of the most sensitive processes to a wide range of abiotic stresses. Because hydraulics and metabolics are two major determinants of expansive growth (volumetric increase) and structural growth (dry matter increase), we review the interaction nodes between water and carbon. We detail the crosstalks between water and carbon transports, including the dual role of stomata and aquaporins in regulating water and carbon fluxes, the coupling between phloem and xylem, the interactions between leaf water relations and photosynthetic capacity, the links between Lockhart's hydromechanical model and carbon metabolism, and the central regulatory role of abscisic acid. Then, we argue that during leaf ontogeny, these interactions change dramatically because of uncoupled modifications between several anatomical and physiological features of the leaf. We conclude that the control of leaf growth switches from a metabolic to a hydromechanical limitation during the course of leaf ontogeny. Finally, we illustrate how taking leaf ontogeny into account provides insights into the mechanisms underlying leaf growth responses to abiotic stresses that affect water and carbon relations, such as elevated CO2, low light, high temperature and drought.

Water: the most important ‘molecular’ component of water stress tolerance research

“…Thus, genotypes that exhibit sensitivity to a high VPD with respect to their leaf area development would have smaller leaf areas than insensitive genotypes if grown under such conditions. It is indeed quite clear that leaf development is under hydraulic control (Munns and Cramer 1996;Tardieu et al 2010;Pantin et al 2012). Leaf development is also sensitive to soil drying, and the termination of leaf growth occurs before termination of transpiration (Sadras and Milroy 1996;Soltani et al 2001;Reymond et al 2003;Parent et al 2009;Tardieu et al 2010).…”

“…Some of these differences are genetic; however, environmental conditions are also known to play an important role in leaf area development through a combination of hydraulic and metabolic controls (Pantin et al 2011(Pantin et al , 2012Kudoyarova et al 2013). For example, maize leaf development varied among genotypes when plants were exposed to either a high vapour pressure deficit (VPD) or a low soil water potential (Reymond et al 2003).…”

Kinematic evidence that atmospheric nitrogen dioxide increases the rates of cell proliferation and enlargement to stimulate leaf expansion in Arabidopsis

“…RLER and RCER decrease, but cell division almost stops during the third phase. 1,11 In -NO 2 plants, the RLER and RCDR curves appeared to be almost constant at 19-21 DAS and slightly decreased at 21-23 DAS ( Fig. 1D and E), which correspond to the characteristics of the first and second phases, respectively, of the leaf expansion model described above.…”

“…1D and E), and therefore lacked features characteristic of the first phase of the model. 1,11 Thus, the first phase may have started earlier than 19 DAS in CNO 2 plants, which is at least 2 days earlier than in -NO 2 plants. In addition, the RCER curve exhibited a peak around 21 DAS (Fig.…”

“…1 Atmospheric nitrogen dioxide (NO 2 ), as a positive growth regulator, stimulates both of these components of leaf growth. We previously reported that NO 2 increases leaf size and shoot biomass by 2.5-fold each.…”