<i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots

Phosphate (Pi) availability has a strong influence on the symbiotic interaction between <i>Arabidopsis</i> and a recently described root-colonizing beneficial <i>Trichoderma harzianum</i> strain. When transferred to media with insoluble Ca<sub>3</sub>(PO<sub>...

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Main Authors: Hamid Rouina, Yu-Heng Tseng, Karaba N. Nataraja, Ramanan Uma Shaanker, Ralf Oelmüller
Format: Article
Language:English
Published: MDPI AG 2021-06-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/9/6/1246
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author Hamid Rouina
Yu-Heng Tseng
Karaba N. Nataraja
Ramanan Uma Shaanker
Ralf Oelmüller
author_facet Hamid Rouina
Yu-Heng Tseng
Karaba N. Nataraja
Ramanan Uma Shaanker
Ralf Oelmüller
author_sort Hamid Rouina
collection DOAJ
description Phosphate (Pi) availability has a strong influence on the symbiotic interaction between <i>Arabidopsis</i> and a recently described root-colonizing beneficial <i>Trichoderma harzianum</i> strain. When transferred to media with insoluble Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> as a sole Pi source, <i>Arabidopsis</i> seedlings died after 10 days. <i>Trichoderma</i> grew on the medium containing Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> and the fungus did colonize in roots, stems, and shoots of the host. The efficiency of the photosynthetic electron transport of the colonized seedlings grown on Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> medium was reduced and the seedlings died earlier, indicating that the fungus exerts an additional stress to the plant. Interestingly, the fungus initially alleviated the Pi starvation response and did not activate defense responses against the hyphal propagation. However, in colonized roots, the sucrose transporter genes <i>SWEET11</i> and -<i>12</i> were strongly down-regulated, restricting the unloading of sucrose from the phloem parenchyma cells to the apoplast. Simultaneously, up-regulation of <i>SUC1</i> promoted sucrose uptake from the apoplast into the parenchyma cells and of <i>SWEET2</i> sequestration of sucrose in the vacuole of the root cells. We propose that the fungus tries to escape from the Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> medium and colonizes the entire host. To prevent excessive sugar consumption by the propagating hyphae, the host restricts sugar availability in its apoplastic root space by downregulating sugar transporter genes for phloem unloading, and by upregulating transporter genes which maintain the sugar in the root cells.
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spelling doaj.art-4fed2be854b846cead2991ea152f1aba2023-11-21T23:17:10ZengMDPI AGMicroorganisms2076-26072021-06-0196124610.3390/microorganisms9061246<i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the RootsHamid Rouina0Yu-Heng Tseng1Karaba N. Nataraja2Ramanan Uma Shaanker3Ralf Oelmüller4Department of Plant Physiology, Matthias Schleiden Institute of Genetics, Bioinformatics and Molecular Botany, Friedrich-Schiller-University Jena, 07743 Jena, GermanyDepartment of Plant Physiology, Matthias Schleiden Institute of Genetics, Bioinformatics and Molecular Botany, Friedrich-Schiller-University Jena, 07743 Jena, GermanyDepartment of Crop Physiology, University of Agricultural Sciences, GKVK, Bangalore 560065, Karnataka, IndiaSchool of Ecology and Conservation, University of Agricultural Sciences, GKVK, Bangalore 560065, Karnataka, IndiaDepartment of Plant Physiology, Matthias Schleiden Institute of Genetics, Bioinformatics and Molecular Botany, Friedrich-Schiller-University Jena, 07743 Jena, GermanyPhosphate (Pi) availability has a strong influence on the symbiotic interaction between <i>Arabidopsis</i> and a recently described root-colonizing beneficial <i>Trichoderma harzianum</i> strain. When transferred to media with insoluble Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> as a sole Pi source, <i>Arabidopsis</i> seedlings died after 10 days. <i>Trichoderma</i> grew on the medium containing Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> and the fungus did colonize in roots, stems, and shoots of the host. The efficiency of the photosynthetic electron transport of the colonized seedlings grown on Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> medium was reduced and the seedlings died earlier, indicating that the fungus exerts an additional stress to the plant. Interestingly, the fungus initially alleviated the Pi starvation response and did not activate defense responses against the hyphal propagation. However, in colonized roots, the sucrose transporter genes <i>SWEET11</i> and -<i>12</i> were strongly down-regulated, restricting the unloading of sucrose from the phloem parenchyma cells to the apoplast. Simultaneously, up-regulation of <i>SUC1</i> promoted sucrose uptake from the apoplast into the parenchyma cells and of <i>SWEET2</i> sequestration of sucrose in the vacuole of the root cells. We propose that the fungus tries to escape from the Ca<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub> medium and colonizes the entire host. To prevent excessive sugar consumption by the propagating hyphae, the host restricts sugar availability in its apoplastic root space by downregulating sugar transporter genes for phloem unloading, and by upregulating transporter genes which maintain the sugar in the root cells.https://www.mdpi.com/2076-2607/9/6/1246<i>Trichoderma</i>SWEET11SWEET12SWEET2SUC1sucrose/sugar transporter
spellingShingle Hamid Rouina
Yu-Heng Tseng
Karaba N. Nataraja
Ramanan Uma Shaanker
Ralf Oelmüller
<i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots
Microorganisms
<i>Trichoderma</i>
SWEET11
SWEET12
SWEET2
SUC1
sucrose/sugar transporter
title <i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots
title_full <i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots
title_fullStr <i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots
title_full_unstemmed <i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots
title_short <i>Arabidopsis</i> Restricts Sugar Loss to a Colonizing <i>Trichoderma harzianum</i> Strain by Downregulating <i>SWEET11</i> and <i>-12</i> and Upregulation of <i>SUC1</i> and <i>SWEET2</i> in the Roots
title_sort i arabidopsis i restricts sugar loss to a colonizing i trichoderma harzianum i strain by downregulating i sweet11 i and i 12 i and upregulation of i suc1 i and i sweet2 i in the roots
topic <i>Trichoderma</i>
SWEET11
SWEET12
SWEET2
SUC1
sucrose/sugar transporter
url https://www.mdpi.com/2076-2607/9/6/1246
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