Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour

<jats:title>Summary</jats:title><jats:p>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<jats:styled-content style="fixed-case">CO</jats:styled-content><jats:sub>2</jats:sub>uptake for photosynthesis (<jats:italic>A</jats:italic>) and water loss, and ultimately plant water use efficiency (<jats:styled-content style="fixed-case">WUE</jats:styled-content>). A strong correlation between<jats:italic>A</jats:italic>and stomatal conductance (<jats:italic>g</jats:italic><jats:sub>s</jats:sub>) 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<jats:styled-content style="fixed-case">WUE</jats:styled-content>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<jats:styled-content style="fixed-case">CO</jats:styled-content><jats:sub>2</jats:sub>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<jats:styled-content style="fixed-case">WUE</jats:styled-content>and crop yield.</jats:p><jats:p><jats:table-wrap position="anchor"><jats:table frame="void"><jats:col width="1"/><jats:col width="1"/><jats:col width="1"/><jats:thead><jats:tr><jats:th/><jats:th>Contents</jats:th><jats:th/></jats:tr></jats:thead><jats:tbody><jats:tr><jats:td/><jats:td>Summary</jats:td><jats:td>1064</jats:td></jats:tr><jats:tr><jats:td>I.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0002">Introduction</jats:ext-link></jats:td><jats:td>1064</jats:td></jats:tr><jats:tr><jats:td>II.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0003">Coordination between mesophyll and stomata</jats:ext-link></jats:td><jats:td>1066</jats:td></jats:tr><jats:tr><jats:td>III.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0004">The mesophyll signal</jats:ext-link></jats:td><jats:td>1066</jats:td></jats:tr><jats:tr><jats:td>IV.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0005">Arguments against a mesophyll‐driven signal other than<jats:italic>C</jats:italic><jats:sub>i</jats:sub></jats:ext-link></jats:td><jats:td>1068</jats:td></jats:tr><jats:tr><jats:td>V.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0006">Guard cell osmoregulation and evidence for a role of sucrose</jats:ext-link></jats:td><jats:td>1069</jats:td></jats:tr><jats:tr><jats:td>VI.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0007">Degradation of starch</jats:ext-link></jats:td><jats:td>1070</jats:td></jats:tr><jats:tr><jats:td>VII.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0008">Guard cell photosynthetic production of Suc</jats:ext-link></jats:td><jats:td>1070</jats:td></jats:tr><jats:tr><jats:td>VIII.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0009">Guard cell Suc imported from the mesophyll</jats:ext-link></jats:td><jats:td>1070</jats:td></jats:tr><jats:tr><jats:td>IX.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0010">Sugar sensing and metabolism</jats:ext-link></jats:td><jats:td>1071</jats:td></jats:tr><jats:tr><jats:td>X.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0011">The importance of malate as a mesophyll‐driven signal</jats:ext-link></jats:td><jats:td>1072</jats:td></jats:tr><jats:tr><jats:td>XI.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0012">Role of aquaporins</jats:ext-link></jats:td><jats:td>1074</jats:td></jats:tr><jats:tr><jats:td>XII.</jats:td><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0013">Guard cell manipulation and possible future directions</jats:ext-link></jats:td><jats:td>1074</jats:td></jats:tr><jats:tr><jats:td/><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-sec-0014">Acknowledgements</jats:ext-link></jats:td><jats:td>1076</jats:td></jats:tr><jats:tr><jats:td/><jats:td><jats:ext-link xmlns:xlink="http://www.w3.org/1999/xlink" xlink:href="#nph12945-bibl-0001">References</jats:ext-link></jats:td><jats:td>1076</jats:td></jats:tr></jats:tbody></jats:table></jats:table-wrap></jats:p>