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

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)

Abstract

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 SWEET1b 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 MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b 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 MtSWEET1bY57A/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 MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

Original languageEnglish
Pages (from-to)396-408
JournalNew Phytologist
Volume224
Issue number1
Early online date31 May 2019
DOIs
Publication statusPublished - Oct 2019

Fingerprint

Medicago truncatula
Symbiosis
symbiosis
transporters
Maintenance
sugars
Glucose
glucose
mycorrhizal fungi
Fungi
mutants
Hexoses
Membranes
Mycelium
hexoses
plant architecture
mycelium
Minerals
root growth
Soil

Keywords

  • arbuscular mycorrhiza (AM)
  • glucose
  • Medicago truncatula
  • sugar export
  • SWEET
  • symbiosis

Cite this

An, Jianyong ; Zeng, Tian ; Ji, Chuanya ; de Graaf, Sanne ; Zheng, Zijun ; Xiao, Ting Ting ; Deng, Xiuxin ; Xiao, Shunyuan ; Bisseling, Ton ; Limpens, Erik ; Pan, Zhiyong. / A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. In: New Phytologist. 2019 ; Vol. 224, No. 1. pp. 396-408.
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abstract = "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 SWEET1b 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 MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b 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 MtSWEET1bY57A/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 MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.",
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author = "Jianyong An and Tian Zeng and Chuanya Ji and {de Graaf}, Sanne and Zijun Zheng and Xiao, {Ting Ting} and Xiuxin Deng and Shunyuan Xiao and Ton Bisseling and Erik Limpens and Zhiyong Pan",
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A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. / An, Jianyong; Zeng, Tian; Ji, Chuanya; de Graaf, Sanne; Zheng, Zijun; Xiao, Ting Ting; Deng, Xiuxin; Xiao, Shunyuan; Bisseling, Ton; Limpens, Erik; Pan, Zhiyong.

In: New Phytologist, Vol. 224, No. 1, 10.2019, p. 396-408.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

AU - An, Jianyong

AU - Zeng, Tian

AU - Ji, Chuanya

AU - de Graaf, Sanne

AU - Zheng, Zijun

AU - Xiao, Ting Ting

AU - Deng, Xiuxin

AU - Xiao, Shunyuan

AU - Bisseling, Ton

AU - Limpens, Erik

AU - Pan, Zhiyong

PY - 2019/10

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N2 - 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 SWEET1b 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 MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b 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 MtSWEET1bY57A/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 MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

AB - 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 SWEET1b 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 MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b 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 MtSWEET1bY57A/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 MtSWEET1b in the transport of glucose across the peri-arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

KW - arbuscular mycorrhiza (AM)

KW - glucose

KW - Medicago truncatula

KW - sugar export

KW - SWEET

KW - symbiosis

U2 - 10.1111/nph.15975

DO - 10.1111/nph.15975

M3 - Article

VL - 224

SP - 396

EP - 408

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

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