Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis

Abstract In Populus and many other tree species, photoassimilate sucrose diffuses down a concentration gradient via symplastically connected mesophyll cells to minor vein phloem for long‐distance transport. There is no evidence for apoplastic phloem‐loading in Populus. However, plasma membrane sucro...

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Main Authors: Liang‐Jiao Xue, Moh'd I. Hozain, Christopher J. Frost, Afraz Talebi, Batbayar Nyamdari, Kavita B. Aulakh, Ran Zhou, Scott A. Harding, Chung‐Jui Tsai
Format: Article
Language:English
Published: Wiley 2025-03-01
Series:Plant Direct
Online Access:https://doi.org/10.1002/pld3.70023
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author Liang‐Jiao Xue
Moh'd I. Hozain
Christopher J. Frost
Afraz Talebi
Batbayar Nyamdari
Kavita B. Aulakh
Ran Zhou
Scott A. Harding
Chung‐Jui Tsai
author_facet Liang‐Jiao Xue
Moh'd I. Hozain
Christopher J. Frost
Afraz Talebi
Batbayar Nyamdari
Kavita B. Aulakh
Ran Zhou
Scott A. Harding
Chung‐Jui Tsai
author_sort Liang‐Jiao Xue
collection DOAJ
description Abstract In Populus and many other tree species, photoassimilate sucrose diffuses down a concentration gradient via symplastically connected mesophyll cells to minor vein phloem for long‐distance transport. There is no evidence for apoplastic phloem‐loading in Populus. However, plasma membrane sucrose transporters (SUT1 and SUT3) orthologous to those associated with apoplastic phloem loading are expressed in vascular tissues of poplar. While SUT3 functions in sucrose import into developing xylem, the role of SUT1 remains unclear. Here, we overexpressed PtaSUT1 in Populus tremula x P. alba to examine the effects on sucrose partitioning in transgenic plants. Overall leaf sucrose levels were similar between wild type and transgenic lines. Stem sucrose levels were not changed in bark but were significantly reduced in the adjacent xylem, suggesting hindered intercellular sucrose trafficking from the phloem to the developing xylem. Fully expanded leaves of transgenic plants deteriorated prematurely with declining photosynthesis prior to severe necrotic spotting. Necrotic spotting advanced most rapidly in the distal portion of mature leaves and was accompanied by sharp hexose increases and sharp sucrose decreases there. Leaf transcriptome profiling and network inference revealed the down‐regulation of copper proteins and elevated expression of copper microRNAs prior to noticeable leaf injury. Our results suggest ectopic expression of PtaSUT1 altered sucrose partitioning in stems with systemic effects on leaf health and copper homeostasis mediated in part by sucrose‐sensitive copper miRNAs.
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spelling doaj-art-6e4f16876ea042e087881a6de7be7a8f2025-07-23T11:16:03ZengWileyPlant Direct2475-44552025-03-0193n/an/a10.1002/pld3.70023Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosisLiang‐Jiao Xue0Moh'd I. Hozain1Christopher J. Frost2Afraz Talebi3Batbayar Nyamdari4Kavita B. Aulakh5Ran Zhou6Scott A. Harding7Chung‐Jui Tsai8Warnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAWarnell School of Forestry and Natural Resources University of Georgia Athens GA USAAbstract In Populus and many other tree species, photoassimilate sucrose diffuses down a concentration gradient via symplastically connected mesophyll cells to minor vein phloem for long‐distance transport. There is no evidence for apoplastic phloem‐loading in Populus. However, plasma membrane sucrose transporters (SUT1 and SUT3) orthologous to those associated with apoplastic phloem loading are expressed in vascular tissues of poplar. While SUT3 functions in sucrose import into developing xylem, the role of SUT1 remains unclear. Here, we overexpressed PtaSUT1 in Populus tremula x P. alba to examine the effects on sucrose partitioning in transgenic plants. Overall leaf sucrose levels were similar between wild type and transgenic lines. Stem sucrose levels were not changed in bark but were significantly reduced in the adjacent xylem, suggesting hindered intercellular sucrose trafficking from the phloem to the developing xylem. Fully expanded leaves of transgenic plants deteriorated prematurely with declining photosynthesis prior to severe necrotic spotting. Necrotic spotting advanced most rapidly in the distal portion of mature leaves and was accompanied by sharp hexose increases and sharp sucrose decreases there. Leaf transcriptome profiling and network inference revealed the down‐regulation of copper proteins and elevated expression of copper microRNAs prior to noticeable leaf injury. Our results suggest ectopic expression of PtaSUT1 altered sucrose partitioning in stems with systemic effects on leaf health and copper homeostasis mediated in part by sucrose‐sensitive copper miRNAs.https://doi.org/10.1002/pld3.70023
spellingShingle Liang‐Jiao Xue
Moh'd I. Hozain
Christopher J. Frost
Afraz Talebi
Batbayar Nyamdari
Kavita B. Aulakh
Ran Zhou
Scott A. Harding
Chung‐Jui Tsai
Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
Plant Direct
title Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
title_full Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
title_fullStr Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
title_full_unstemmed Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
title_short Overexpression of plasma membrane SUT1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
title_sort overexpression of plasma membrane sut1 in poplar alters lateral sucrose partitioning in stem and promotes leaf necrosis
url https://doi.org/10.1002/pld3.70023
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