2019New PhytologistOpen access

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Jianyong An, Tian Zeng, Chuanya Ji, Sanne de Graaf, Zijun Zheng, Ting Ting Xiao, Xiuxin Deng, Shunyuan Xiao, Ton Bisseling, Erik Limpens, Zhiyong Pan

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Abstract

Summary Plants form a mutualistic symbiosis with arbuscular mycorrhizal ( AM ) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula . We show that M. truncatula SWEET 1b transporter is strongly upregulated in arbuscule‐containing cells compared to roots and localizes to the peri‐arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of Mt SWEET 1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of Mt SWEET 1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule‐specific overexpression of Mt SWEET 1b Y57A/G58D , which are considered to act in a dominant‐negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for Mt SWEET 1b in the transport of glucose across the peri‐arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

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Summary Plants form a mutualistic symbiosis with arbuscular mycorrhizal ( AM ) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula . We show that M. truncatula SWEET 1b transporter is strongly upregulated in arbuscule‐containing cells compared to roots and localizes to the peri‐arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of Mt SWEET 1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of Mt SWEET 1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule‐specific overexpression of Mt SWEET 1b Y57A/G58D , which are considered to act in a dominant‐negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for Mt SWEET 1b in the transport of glucose across the peri‐arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

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Available abstract

Summary Plants form a mutualistic symbiosis with arbuscular mycorrhizal ( AM ) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula . We show that M. truncatula SWEET 1b transporter is strongly upregulated in arbuscule‐containing cells compared to roots and localizes to the peri‐arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of Mt SWEET 1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of Mt SWEET 1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule‐specific overexpression of Mt SWEET 1b Y57A/G58D , which are considered to act in a dominant‐negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for Mt SWEET 1b in the transport of glucose across the peri‐arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

Key concepts: Medicago truncatula, Symbiosis, Rhizophagus irregularis, Biology, Endosymbiosis, Mutant, Mycelium, Arbuscular mycorrhiza

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