External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum

Aluminium (Al) is toxic to most plants, but recent research has suggested that Al addition may stimulate growth and nutrient uptake in some species capable of accumulating high tissue Al concentrations. The physiological basis of this growth response is unknown, but it may be associated with process...

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Main Authors: Ali, Sajid, Mahmud, Khairil, Weitz, Hedda, H. Kritzler, Ully, Burslem, David F. R. P.
Format: Article
Language:English
Published: Public Library of Science 2024
Online Access:http://psasir.upm.edu.my/id/eprint/112090/1/journal.pone.0297686.pdf
http://psasir.upm.edu.my/id/eprint/112090/
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0297686
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spelling my.upm.eprints.1120902024-10-23T07:38:18Z http://psasir.upm.edu.my/id/eprint/112090/ External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum Ali, Sajid Mahmud, Khairil Weitz, Hedda H. Kritzler, Ully Burslem, David F. R. P. Aluminium (Al) is toxic to most plants, but recent research has suggested that Al addition may stimulate growth and nutrient uptake in some species capable of accumulating high tissue Al concentrations. The physiological basis of this growth response is unknown, but it may be associated with processes linked to the regulation of carbon assimilation and partitioning by Al supply. To test alternative hypotheses for the physiological mechanism explaining this response, we examined the effects of increasing Al concentrations in the growth medium on tissue nutrient concentrations and carbon assimilation in two populations of the Al-accumulator Melastoma malabathricum. Compared to seedlings grown in a control nutrient solution containing no Al, mean rates of photosynthesis and respiration increased by 46% and 27%, respectively, total non-structural carbohydrate concentrations increased by 45%, and lignin concentration in roots decreased by 26% when seedlings were grown in a nutrient solution containing 2.0 mM Al. The concentrations of P, Ca and Mg in leaves and stems increased by 31%, 22%, and 26%, respectively, in response to an increase in nutrient solution Al concentration from 0 to 2.0 mM. Elemental concentrations in roots increased for P (114%), Mg (61%) and K (5%) in response to this increase in Al concentration in the nutrient solution. Plants derived from an inherently faster-growing population had a greater relative increase in final dry mass, net photosynthetic and respiration rates and total non-structural carbohydrate concentrations in response to higher external Al supply. We conclude that growth stimulation by Al supply is associated with increases in photosynthetic and respiration rates and enhanced production of non-structural carbohydrates that are differentially allocated to roots, as well as stimulation of nutrient uptake. These responses suggest that internal carbon assimilation is up-regulated to provide the necessary resources of non-structural carbohydrates for uptake, transport and storage of Al in Melastoma malabathricum. This physiological mechanism has only been recorded previously in one other plant species, Camellia sinensis, which last shared a common ancestor with M. malabathricum more than 120 million years ago. Public Library of Science 2024 Article PeerReviewed text en http://psasir.upm.edu.my/id/eprint/112090/1/journal.pone.0297686.pdf Ali, Sajid and Mahmud, Khairil and Weitz, Hedda and H. Kritzler, Ully and Burslem, David F. R. P. (2024) External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum. PLoS ONE, 19 (3). e0297686. ISSN 1932-6203 https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0297686 10.1371/journal.pone.0297686
institution Universiti Putra Malaysia
building UPM Library
collection Institutional Repository
continent Asia
country Malaysia
content_provider Universiti Putra Malaysia
content_source UPM Institutional Repository
url_provider http://psasir.upm.edu.my/
language English
description Aluminium (Al) is toxic to most plants, but recent research has suggested that Al addition may stimulate growth and nutrient uptake in some species capable of accumulating high tissue Al concentrations. The physiological basis of this growth response is unknown, but it may be associated with processes linked to the regulation of carbon assimilation and partitioning by Al supply. To test alternative hypotheses for the physiological mechanism explaining this response, we examined the effects of increasing Al concentrations in the growth medium on tissue nutrient concentrations and carbon assimilation in two populations of the Al-accumulator Melastoma malabathricum. Compared to seedlings grown in a control nutrient solution containing no Al, mean rates of photosynthesis and respiration increased by 46% and 27%, respectively, total non-structural carbohydrate concentrations increased by 45%, and lignin concentration in roots decreased by 26% when seedlings were grown in a nutrient solution containing 2.0 mM Al. The concentrations of P, Ca and Mg in leaves and stems increased by 31%, 22%, and 26%, respectively, in response to an increase in nutrient solution Al concentration from 0 to 2.0 mM. Elemental concentrations in roots increased for P (114%), Mg (61%) and K (5%) in response to this increase in Al concentration in the nutrient solution. Plants derived from an inherently faster-growing population had a greater relative increase in final dry mass, net photosynthetic and respiration rates and total non-structural carbohydrate concentrations in response to higher external Al supply. We conclude that growth stimulation by Al supply is associated with increases in photosynthetic and respiration rates and enhanced production of non-structural carbohydrates that are differentially allocated to roots, as well as stimulation of nutrient uptake. These responses suggest that internal carbon assimilation is up-regulated to provide the necessary resources of non-structural carbohydrates for uptake, transport and storage of Al in Melastoma malabathricum. This physiological mechanism has only been recorded previously in one other plant species, Camellia sinensis, which last shared a common ancestor with M. malabathricum more than 120 million years ago.
format Article
author Ali, Sajid
Mahmud, Khairil
Weitz, Hedda
H. Kritzler, Ully
Burslem, David F. R. P.
spellingShingle Ali, Sajid
Mahmud, Khairil
Weitz, Hedda
H. Kritzler, Ully
Burslem, David F. R. P.
External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum
author_facet Ali, Sajid
Mahmud, Khairil
Weitz, Hedda
H. Kritzler, Ully
Burslem, David F. R. P.
author_sort Ali, Sajid
title External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum
title_short External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum
title_full External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum
title_fullStr External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum
title_full_unstemmed External aluminium supply regulates photosynthesis and carbon partitioning in the Al-accumulating tropical shrub Melastoma malabathricum
title_sort external aluminium supply regulates photosynthesis and carbon partitioning in the al-accumulating tropical shrub melastoma malabathricum
publisher Public Library of Science
publishDate 2024
url http://psasir.upm.edu.my/id/eprint/112090/1/journal.pone.0297686.pdf
http://psasir.upm.edu.my/id/eprint/112090/
https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0297686
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