Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour

Summary Stomata control gaseous fluxes between the internal leaf air spaces and the external atmosphere. Guard cells determine stomatal aperture and must operate to ensure an appropriate balance between CO 2 uptake for photosynthesis ( A ) and water loss, and ultimately plant water use efficiency ( WUE ). A strong correlation between A and stomatal conductance ( g s ) is well documented and often observed, but the underlying mechanisms, possible signals and metabolites that promote this relationship are currently unknown. In this review we evaluate the current literature on mesophyll‐driven signals that may coordinate stomatal behaviour with mesophyll carbon assimilation. We explore a possible role of various metabolites including sucrose and malate (from several potential sources; including guard cell photosynthesis) and new evidence that improvements in WUE have been made by manipulating sucrose metabolism within the guard cells. Finally we discuss the new tools and techniques available for potentially manipulating cell‐specific metabolism, including guard and mesophyll cells, in order to elucidate mesophyll‐derived signals that coordinate mesophyll CO 2 demands with stomatal behaviour, in order to provide a mechanistic understanding of these processes as this may identify potential targets for manipulations in order to improve plant WUE and crop yield. Contents Summary 1064 I. Introduction 1064 II. Coordination between mesophyll and stomata 1066 III. The mesophyll signal 1066 IV. Arguments against a mesophyll‐driven signal other than C i 1068 V. Guard cell osmoregulation and evidence for a role of sucrose 1069 VI. Degradation of starch 1070 VII. Guard cell photosynthetic production of Suc 1070 VIII. Guard cell Suc imported from the mesophyll 1070 IX. Sugar sensing and metabolism 1071 X. The importance of malate as a mesophyll‐driven signal 1072 XI. Role of aquaporins 1074 XII. Guard cell manipulation and possible future directions 1074 Acknowledgements 1076 References 1076