Two members of the aluminum-activated malate transporter family, SlALMT4 and SlALMT5, are expressed during fruit development, and the overexpression of SlALMT5 alters organic acid contents in seeds in tomato (Solanum lycopersicum)

Takayuki Sasaki, Yoshiyuki Tsuchiya, Michiyo Ariyoshi, Ryohei Nakano, Koichiro Ushijima, Yasutaka Kubo, Izumi Mori, Emi Higashiizumi, Ivan Galis, Yoko Yamamoto

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Abstract

The aluminum-activated malate transporter (ALMT) family of proteins transports malate and/or inorganic anions across plant membranes. To demonstrate the possible role of ALMT genes in tomato fruit development, we focused on SlALMT4 and SlALMT5, the two major genes expressed during fruit development. Predicted proteins were classified into clade 2 of the family, many members of which localize to endomembranes. Tissue-specific gene expression was determined using transgenic tomato expressing the b-glucuronidase reporter gene controlled by their own promoters. Both the genes were expressed in vascular bundles connecting to developing seeds in fruit and in the embryo of mature seeds. Further, SlALMT5 was expressed in embryo in developing seeds in fruit. Subcellular localization of both proteins to the endoplasmic reticulum (ER) was established by transiently expressing the green fluorescent protein fusions in plant protoplasts. SlALMT5 probably localized to other endomembranes as well. Localization of SlALMT5 to the ER was also confirmed by immunoblot analysis. The transport function of both SlALMT proteins was investigated electrophysiologically in Xenopus oocytes. SlALMT5 transported malate and inorganic anions such as nitrate and chloride, but not citrate. SlALMT4 also transported malate, but the results were less consistent perhaps because it did not localize strongly to the plasma membrane. To elucidate the physiological role of SlALMT5 further, we overexpressed SlALMT5 in tomato. Compared with the wild type, overexpressors exhibited higher malate and citrate contents in mature seeds, but not in fruit. We conclude that the malate transport function of SlALMT5 expressed in developing fruit influences the organic acid contents in mature seeds.

Original languageEnglish
Pages (from-to)2367-2379
Number of pages13
JournalPlant and Cell Physiology
Volume57
Issue number11
DOIs
Publication statusPublished - Nov 1 2016

Fingerprint

Solanum lycopersicum
malates
Lycopersicon esculentum
Aluminum
organic acids and salts
aluminum
fruiting
transporters
Fruit
Seeds
tomatoes
Acids
seeds
fruits
Citric Acid
citrates
embryo (plant)
Endoplasmic Reticulum
anions
endoplasmic reticulum

Keywords

  • Aluminum-activated malate transporter
  • Endomembrane
  • Fruit development
  • Organic acid
  • Seed
  • Tomato.edited-statecorrected-proof

ASJC Scopus subject areas

  • Medicine(all)
  • Physiology
  • Plant Science
  • Cell Biology

Cite this

@article{f1437588ae2148028f1affc4312a2a3d,
title = "Two members of the aluminum-activated malate transporter family, SlALMT4 and SlALMT5, are expressed during fruit development, and the overexpression of SlALMT5 alters organic acid contents in seeds in tomato (Solanum lycopersicum)",
abstract = "The aluminum-activated malate transporter (ALMT) family of proteins transports malate and/or inorganic anions across plant membranes. To demonstrate the possible role of ALMT genes in tomato fruit development, we focused on SlALMT4 and SlALMT5, the two major genes expressed during fruit development. Predicted proteins were classified into clade 2 of the family, many members of which localize to endomembranes. Tissue-specific gene expression was determined using transgenic tomato expressing the b-glucuronidase reporter gene controlled by their own promoters. Both the genes were expressed in vascular bundles connecting to developing seeds in fruit and in the embryo of mature seeds. Further, SlALMT5 was expressed in embryo in developing seeds in fruit. Subcellular localization of both proteins to the endoplasmic reticulum (ER) was established by transiently expressing the green fluorescent protein fusions in plant protoplasts. SlALMT5 probably localized to other endomembranes as well. Localization of SlALMT5 to the ER was also confirmed by immunoblot analysis. The transport function of both SlALMT proteins was investigated electrophysiologically in Xenopus oocytes. SlALMT5 transported malate and inorganic anions such as nitrate and chloride, but not citrate. SlALMT4 also transported malate, but the results were less consistent perhaps because it did not localize strongly to the plasma membrane. To elucidate the physiological role of SlALMT5 further, we overexpressed SlALMT5 in tomato. Compared with the wild type, overexpressors exhibited higher malate and citrate contents in mature seeds, but not in fruit. We conclude that the malate transport function of SlALMT5 expressed in developing fruit influences the organic acid contents in mature seeds.",
keywords = "Aluminum-activated malate transporter, Endomembrane, Fruit development, Organic acid, Seed, Tomato.edited-statecorrected-proof",
author = "Takayuki Sasaki and Yoshiyuki Tsuchiya and Michiyo Ariyoshi and Ryohei Nakano and Koichiro Ushijima and Yasutaka Kubo and Izumi Mori and Emi Higashiizumi and Ivan Galis and Yoko Yamamoto",
year = "2016",
month = "11",
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language = "English",
volume = "57",
pages = "2367--2379",
journal = "Plant and Cell Physiology",
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TY - JOUR

T1 - Two members of the aluminum-activated malate transporter family, SlALMT4 and SlALMT5, are expressed during fruit development, and the overexpression of SlALMT5 alters organic acid contents in seeds in tomato (Solanum lycopersicum)

AU - Sasaki, Takayuki

AU - Tsuchiya, Yoshiyuki

AU - Ariyoshi, Michiyo

AU - Nakano, Ryohei

AU - Ushijima, Koichiro

AU - Kubo, Yasutaka

AU - Mori, Izumi

AU - Higashiizumi, Emi

AU - Galis, Ivan

AU - Yamamoto, Yoko

PY - 2016/11/1

Y1 - 2016/11/1

N2 - The aluminum-activated malate transporter (ALMT) family of proteins transports malate and/or inorganic anions across plant membranes. To demonstrate the possible role of ALMT genes in tomato fruit development, we focused on SlALMT4 and SlALMT5, the two major genes expressed during fruit development. Predicted proteins were classified into clade 2 of the family, many members of which localize to endomembranes. Tissue-specific gene expression was determined using transgenic tomato expressing the b-glucuronidase reporter gene controlled by their own promoters. Both the genes were expressed in vascular bundles connecting to developing seeds in fruit and in the embryo of mature seeds. Further, SlALMT5 was expressed in embryo in developing seeds in fruit. Subcellular localization of both proteins to the endoplasmic reticulum (ER) was established by transiently expressing the green fluorescent protein fusions in plant protoplasts. SlALMT5 probably localized to other endomembranes as well. Localization of SlALMT5 to the ER was also confirmed by immunoblot analysis. The transport function of both SlALMT proteins was investigated electrophysiologically in Xenopus oocytes. SlALMT5 transported malate and inorganic anions such as nitrate and chloride, but not citrate. SlALMT4 also transported malate, but the results were less consistent perhaps because it did not localize strongly to the plasma membrane. To elucidate the physiological role of SlALMT5 further, we overexpressed SlALMT5 in tomato. Compared with the wild type, overexpressors exhibited higher malate and citrate contents in mature seeds, but not in fruit. We conclude that the malate transport function of SlALMT5 expressed in developing fruit influences the organic acid contents in mature seeds.

AB - The aluminum-activated malate transporter (ALMT) family of proteins transports malate and/or inorganic anions across plant membranes. To demonstrate the possible role of ALMT genes in tomato fruit development, we focused on SlALMT4 and SlALMT5, the two major genes expressed during fruit development. Predicted proteins were classified into clade 2 of the family, many members of which localize to endomembranes. Tissue-specific gene expression was determined using transgenic tomato expressing the b-glucuronidase reporter gene controlled by their own promoters. Both the genes were expressed in vascular bundles connecting to developing seeds in fruit and in the embryo of mature seeds. Further, SlALMT5 was expressed in embryo in developing seeds in fruit. Subcellular localization of both proteins to the endoplasmic reticulum (ER) was established by transiently expressing the green fluorescent protein fusions in plant protoplasts. SlALMT5 probably localized to other endomembranes as well. Localization of SlALMT5 to the ER was also confirmed by immunoblot analysis. The transport function of both SlALMT proteins was investigated electrophysiologically in Xenopus oocytes. SlALMT5 transported malate and inorganic anions such as nitrate and chloride, but not citrate. SlALMT4 also transported malate, but the results were less consistent perhaps because it did not localize strongly to the plasma membrane. To elucidate the physiological role of SlALMT5 further, we overexpressed SlALMT5 in tomato. Compared with the wild type, overexpressors exhibited higher malate and citrate contents in mature seeds, but not in fruit. We conclude that the malate transport function of SlALMT5 expressed in developing fruit influences the organic acid contents in mature seeds.

KW - Aluminum-activated malate transporter

KW - Endomembrane

KW - Fruit development

KW - Organic acid

KW - Seed

KW - Tomato.edited-statecorrected-proof

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DO - 10.1093/pcp/pcw157

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