Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress

Liverwort Marchantia polymorpha is considered as the key species for addressing a myriad of questions in plant biology. Exploration of drought tolerance mechanism(s) in this group of land plants offers a platform to identify the early adaptive mechanisms involved in drought tolerance. The current st...

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Main Authors: Totan Kumar Ghosh, Naznin Haque Tompa, Md. Mezanur Rahman, Mohammed Mohi-Ud-Din, S. M. Zubair Al-Meraj, Md. Sanaullah Biswas, Mohammad Golam Mostofa
Format: Article
Language:English
Published: PeerJ Inc. 2021-11-01
Series:PeerJ
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Online Access:https://peerj.com/articles/12419.pdf
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author Totan Kumar Ghosh
Naznin Haque Tompa
Md. Mezanur Rahman
Mohammed Mohi-Ud-Din
S. M. Zubair Al-Meraj
Md. Sanaullah Biswas
Mohammad Golam Mostofa
author_facet Totan Kumar Ghosh
Naznin Haque Tompa
Md. Mezanur Rahman
Mohammed Mohi-Ud-Din
S. M. Zubair Al-Meraj
Md. Sanaullah Biswas
Mohammad Golam Mostofa
author_sort Totan Kumar Ghosh
collection DOAJ
description Liverwort Marchantia polymorpha is considered as the key species for addressing a myriad of questions in plant biology. Exploration of drought tolerance mechanism(s) in this group of land plants offers a platform to identify the early adaptive mechanisms involved in drought tolerance. The current study aimed at elucidating the drought acclimation mechanisms in liverwort’s model M. polymorpha. The gemmae, asexual reproductive units of M. polymorpha, were exposed to sucrose (0.2 M), mannitol (0.5 M) and polyethylene glycol (PEG, 10%) for inducing physiological drought to investigate their effects at morphological, physiological and biochemical levels. Our results showed that drought exposure led to extreme growth inhibition, disruption of membrane stability and reduction in photosynthetic pigment contents in M. polymorpha. The increased accumulation of hydrogen peroxide and malondialdehyde, and the rate of electrolyte leakage in the gemmalings of M. polymorpha indicated an evidence of drought-caused oxidative stress. The gemmalings showed significant induction of the activities of key antioxidant enzymes, including superoxide dismutase, catalase, ascorbate peroxidase, dehydroascorbate reductase and glutathione S-transferase, and total antioxidant activity in response to increased oxidative stress under drought. Importantly, to counteract the drought effects, the gemmalings also accumulated a significant amount of proline, which coincided with the evolutionary presence of proline biosynthesis gene Δ1-pyrroline-5-carboxylate synthase 1 (P5CS1) in land plants. Furthermore, the application of exogenous abscisic acid (ABA) reduced drought-induced tissue damage and improved the activities of antioxidant enzymes and accumulation of proline, implying an archetypal role of this phytohormone in M. polymorpha for drought tolerance. We conclude that physiological drought tolerance mechanisms governed by the cellular antioxidants, proline and ABA were adopted in liverwort M. polymorpha, and that these findings have important implications in aiding our understanding of osmotic stress acclimation processes in land plants.
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spelling doaj.art-b152e2aa70fd487fb810c96c76b804332023-12-03T11:33:22ZengPeerJ Inc.PeerJ2167-83592021-11-019e1241910.7717/peerj.12419Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stressTotan Kumar Ghosh0Naznin Haque Tompa1Md. Mezanur Rahman2Mohammed Mohi-Ud-Din3S. M. Zubair Al-Meraj4Md. Sanaullah Biswas5Mohammad Golam Mostofa6Department of Crop Botany, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, BangladeshDepartment of Crop Botany, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, BangladeshInstitute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, Texas, United StatesDepartment of Crop Botany, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, BangladeshDepartment of Crop Botany, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, BangladeshDepartment of Horticulture, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, BangladeshInstitute of Genomics for Crop Abiotic Stress Tolerance, Department of Plant and Soil Science, Texas Tech University, Lubbock, Texas, United StatesLiverwort Marchantia polymorpha is considered as the key species for addressing a myriad of questions in plant biology. Exploration of drought tolerance mechanism(s) in this group of land plants offers a platform to identify the early adaptive mechanisms involved in drought tolerance. The current study aimed at elucidating the drought acclimation mechanisms in liverwort’s model M. polymorpha. The gemmae, asexual reproductive units of M. polymorpha, were exposed to sucrose (0.2 M), mannitol (0.5 M) and polyethylene glycol (PEG, 10%) for inducing physiological drought to investigate their effects at morphological, physiological and biochemical levels. Our results showed that drought exposure led to extreme growth inhibition, disruption of membrane stability and reduction in photosynthetic pigment contents in M. polymorpha. The increased accumulation of hydrogen peroxide and malondialdehyde, and the rate of electrolyte leakage in the gemmalings of M. polymorpha indicated an evidence of drought-caused oxidative stress. The gemmalings showed significant induction of the activities of key antioxidant enzymes, including superoxide dismutase, catalase, ascorbate peroxidase, dehydroascorbate reductase and glutathione S-transferase, and total antioxidant activity in response to increased oxidative stress under drought. Importantly, to counteract the drought effects, the gemmalings also accumulated a significant amount of proline, which coincided with the evolutionary presence of proline biosynthesis gene Δ1-pyrroline-5-carboxylate synthase 1 (P5CS1) in land plants. Furthermore, the application of exogenous abscisic acid (ABA) reduced drought-induced tissue damage and improved the activities of antioxidant enzymes and accumulation of proline, implying an archetypal role of this phytohormone in M. polymorpha for drought tolerance. We conclude that physiological drought tolerance mechanisms governed by the cellular antioxidants, proline and ABA were adopted in liverwort M. polymorpha, and that these findings have important implications in aiding our understanding of osmotic stress acclimation processes in land plants.https://peerj.com/articles/12419.pdfAbscisic acidAntioxidant systemDrought acclimationM. polymorphaMembrane damageOxidative stress
spellingShingle Totan Kumar Ghosh
Naznin Haque Tompa
Md. Mezanur Rahman
Mohammed Mohi-Ud-Din
S. M. Zubair Al-Meraj
Md. Sanaullah Biswas
Mohammad Golam Mostofa
Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress
PeerJ
Abscisic acid
Antioxidant system
Drought acclimation
M. polymorpha
Membrane damage
Oxidative stress
title Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress
title_full Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress
title_fullStr Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress
title_full_unstemmed Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress
title_short Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress
title_sort acclimation of liverwort marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes proline and abscisic acid in land plant adaptation to osmotic stress
topic Abscisic acid
Antioxidant system
Drought acclimation
M. polymorpha
Membrane damage
Oxidative stress
url https://peerj.com/articles/12419.pdf
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