Direct comparison of leaf plasmodesma structure and function in relation to phloem-loading type

Johannes Liesche; Chen Gao; Piotr Binczycki; Signe R. Andersen; Hanna Rademaker; Alexander Schulz; Helle Juel Martens

doi:10.1104/pp.18.01353

Direct comparison of leaf plasmodesma structure and function in relation to phloem-loading type

Johannes Liesche, Chen Gao, Piotr Binczycki, Signe R. Andersen, Hanna Rademaker, Alexander Schulz, Helle Juel Martens

Section for Transport Biology

Abstract

The export of photosynthetically produced sugars from leaves depends on plasmodesmatal transport of sugar molecules from mesophyll to phloem. Traditionally, the density of plasmodesmata (PD) along this phloem-loading pathway has been used as a defining feature of different phloem-loading types, with species proposed to have either many or few PD between the phloem and surrounding cells of the leaf. However, quantitative determination of PD density has rarely been performed. Moreover, the structure of PD has not been considered, even though it could impact permeability, and functional data are only available for very few species. Here, a comparison of PD density, structure, and function using data from transmission electron microscopy and live-cell microscopy was conducted for all relevant cell–cell interfaces in leaves of nine species. These species represent the three principal phloem-loading types currently discussed in literature. Results show that relative PD density among the different cell-cell interfaces in one species, but not absolute PD density, is indicative of phloem-loading type. PD density data of single interfaces, even combined with PD diameter and length data, did not correlate with the intercellular diffusion capacity measured by the fluorescence loss in photobleaching method. This means that PD substructure not visible on standard transmission electron micrographs may have a strong influence on permeability. Furthermore, the results support a proposed passive symplasmic loading mechanism in the tree species horse chestnut (Aesculus hippocastanum), white birch (Betula pubescens), orchard apple (Malus domestica), and gray poplar (Populus x canescens) as functional cell coupling and PD structure differed from active symplasmic and apoplasmic phloem-loading species.

Original language	English
Journal	Plant Physiology
Volume	179
Issue number	4
Pages (from-to)	1768-1778
Number of pages	11
ISSN	0032-0889
DOIs	https://doi.org/10.1104/pp.18.01353
Publication status	Published - 1 Apr 2019

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@article{79424f37370e4377956b69e53d232830,

title = "Direct comparison of leaf plasmodesma structure and function in relation to phloem-loading type",

abstract = "The export of photosynthetically produced sugars from leaves depends on plasmodesmatal transport of sugar molecules from mesophyll to phloem. Traditionally, the density of plasmodesmata (PD) along this phloem-loading pathway has been used as a defining feature of different phloem-loading types, with species proposed to have either many or few PD between the phloem and surrounding cells of the leaf. However, quantitative determination of PD density has rarely been performed. Moreover, the structure of PD has not been considered, even though it could impact permeability, and functional data are only available for very few species. Here, a comparison of PD density, structure, and function using data from transmission electron microscopy and live-cell microscopy was conducted for all relevant cell–cell interfaces in leaves of nine species. These species represent the three principal phloem-loading types currently discussed in literature. Results show that relative PD density among the different cell-cell interfaces in one species, but not absolute PD density, is indicative of phloem-loading type. PD density data of single interfaces, even combined with PD diameter and length data, did not correlate with the intercellular diffusion capacity measured by the fluorescence loss in photobleaching method. This means that PD substructure not visible on standard transmission electron micrographs may have a strong influence on permeability. Furthermore, the results support a proposed passive symplasmic loading mechanism in the tree species horse chestnut (Aesculus hippocastanum), white birch (Betula pubescens), orchard apple (Malus domestica), and gray poplar (Populus x canescens) as functional cell coupling and PD structure differed from active symplasmic and apoplasmic phloem-loading species.",

author = "Johannes Liesche and Chen Gao and Piotr Binczycki and Andersen, {Signe R.} and Hanna Rademaker and Alexander Schulz and Martens, {Helle Juel}",

year = "2019",

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doi = "10.1104/pp.18.01353",

language = "English",

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T1 - Direct comparison of leaf plasmodesma structure and function in relation to phloem-loading type

AU - Liesche, Johannes

AU - Gao, Chen

AU - Binczycki, Piotr

AU - Andersen, Signe R.

AU - Rademaker, Hanna

AU - Schulz, Alexander

AU - Martens, Helle Juel

PY - 2019/4/1

Y1 - 2019/4/1

N2 - The export of photosynthetically produced sugars from leaves depends on plasmodesmatal transport of sugar molecules from mesophyll to phloem. Traditionally, the density of plasmodesmata (PD) along this phloem-loading pathway has been used as a defining feature of different phloem-loading types, with species proposed to have either many or few PD between the phloem and surrounding cells of the leaf. However, quantitative determination of PD density has rarely been performed. Moreover, the structure of PD has not been considered, even though it could impact permeability, and functional data are only available for very few species. Here, a comparison of PD density, structure, and function using data from transmission electron microscopy and live-cell microscopy was conducted for all relevant cell–cell interfaces in leaves of nine species. These species represent the three principal phloem-loading types currently discussed in literature. Results show that relative PD density among the different cell-cell interfaces in one species, but not absolute PD density, is indicative of phloem-loading type. PD density data of single interfaces, even combined with PD diameter and length data, did not correlate with the intercellular diffusion capacity measured by the fluorescence loss in photobleaching method. This means that PD substructure not visible on standard transmission electron micrographs may have a strong influence on permeability. Furthermore, the results support a proposed passive symplasmic loading mechanism in the tree species horse chestnut (Aesculus hippocastanum), white birch (Betula pubescens), orchard apple (Malus domestica), and gray poplar (Populus x canescens) as functional cell coupling and PD structure differed from active symplasmic and apoplasmic phloem-loading species.

AB - The export of photosynthetically produced sugars from leaves depends on plasmodesmatal transport of sugar molecules from mesophyll to phloem. Traditionally, the density of plasmodesmata (PD) along this phloem-loading pathway has been used as a defining feature of different phloem-loading types, with species proposed to have either many or few PD between the phloem and surrounding cells of the leaf. However, quantitative determination of PD density has rarely been performed. Moreover, the structure of PD has not been considered, even though it could impact permeability, and functional data are only available for very few species. Here, a comparison of PD density, structure, and function using data from transmission electron microscopy and live-cell microscopy was conducted for all relevant cell–cell interfaces in leaves of nine species. These species represent the three principal phloem-loading types currently discussed in literature. Results show that relative PD density among the different cell-cell interfaces in one species, but not absolute PD density, is indicative of phloem-loading type. PD density data of single interfaces, even combined with PD diameter and length data, did not correlate with the intercellular diffusion capacity measured by the fluorescence loss in photobleaching method. This means that PD substructure not visible on standard transmission electron micrographs may have a strong influence on permeability. Furthermore, the results support a proposed passive symplasmic loading mechanism in the tree species horse chestnut (Aesculus hippocastanum), white birch (Betula pubescens), orchard apple (Malus domestica), and gray poplar (Populus x canescens) as functional cell coupling and PD structure differed from active symplasmic and apoplasmic phloem-loading species.

UR - http://www.mendeley.com/research/direct-comparison-leaf-plasmodesma-structure-function-relation-phloemloading-type

U2 - 10.1104/pp.18.01353

DO - 10.1104/pp.18.01353

M3 - Journal article

SN - 0032-0889

VL - 179

SP - 1768

EP - 1778

JO - Plant Physiology

JF - Plant Physiology

IS - 4

ER -

Direct comparison of leaf plasmodesma structure and function in relation to phloem-loading type

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