The Arabidopsis vacuolar sugar transporter <scp>SWEET</scp>2 limits carbon sequestration from roots and restricts <i>Pythium</i> infection

<jats:title>Summary</jats:title><jats:p>Plant roots secrete a significant portion of their assimilated carbon into the rhizosphere. The putative sugar transporter <jats:italic><jats:styled-content style="fixed-case">SWEET</jats:styled-content>2</jats:italic> is highly expressed in Arabidopsis roots. Expression patterns of <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2–β‐glucuronidase fusions confirmed that <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2 accumulates highly in root cells and thus may contribute to sugar secretion, specifically from epidermal cells of the root apex. <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2–green fluorescent protein fusions localized to the tonoplast, which engulfs the major sugar storage compartment. Functional analysis of <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2 activity in yeast showed low uptake activity for the glucose analog 2‐deoxyglucose, consistent with a role in the transport of glucose across the tonoplast. Loss‐of‐function <jats:italic>sweet2</jats:italic> mutants showed reduced tolerance to excess glucose, lower glucose accumulation in leaves, and 15–25% higher glucose‐derived carbon efflux from roots, suggesting that <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2 has a role in preventing the loss of sugar from root tissue. <jats:italic><jats:styled-content style="fixed-case">SWEET</jats:styled-content></jats:italic>2 root expression was induced more than 10‐fold during <jats:italic>Pythium</jats:italic> infection. Importantly, <jats:italic>sweet2</jats:italic> mutants were more susceptible to the oomycete, showing impaired growth after infection. We propose that root‐expressed vacuolar <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2 modulates sugar secretion, possibly by reducing the availability of glucose sequestered in the vacuole, thereby limiting carbon loss to the rhizosphere. Moreover, the reduced availability of sugar in the rhizosphere due to <jats:styled-content style="fixed-case">SWEET</jats:styled-content>2 activity contributes to resistance to <jats:italic>Pythium</jats:italic>.</jats:p>