Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock

Phosphorus (P) is an essential macronutrient for plant growth, but its availability in soil is often insufficient to achieve optimum crop yield. The As-hyperaccumulator Pteris vittata thrives under low-P condition, with the underlying mechanisms remaining unclear. To understand the P-scavenging trai...

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Main Authors: Chun-Yan Hu, Shufen Xiao, Daniel Menezes-Blackburn, Benjamin L. Turner, Yue Cao, Chenjing Liu, Lena Q. Ma
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Soil & Environmental Health
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Online Access:http://www.sciencedirect.com/science/article/pii/S2949919425000317
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author Chun-Yan Hu
Shufen Xiao
Daniel Menezes-Blackburn
Benjamin L. Turner
Yue Cao
Chenjing Liu
Lena Q. Ma
author_facet Chun-Yan Hu
Shufen Xiao
Daniel Menezes-Blackburn
Benjamin L. Turner
Yue Cao
Chenjing Liu
Lena Q. Ma
author_sort Chun-Yan Hu
collection DOAJ
description Phosphorus (P) is an essential macronutrient for plant growth, but its availability in soil is often insufficient to achieve optimum crop yield. The As-hyperaccumulator Pteris vittata thrives under low-P condition, with the underlying mechanisms remaining unclear. To understand the P-scavenging traits of P. vittata, we grew P vittata under three P-limiting conditions, low soluble-P, calcium phytate (insoluble organic P), and phosphate rock (PR; insoluble inorganic P), to quantify plant growth, As and P uptake, root exudates, and the gene expression of P transporters. Plants were grown under hydroponics with 50 ​μM As and 20 ​μM soluble-P, 2000 ​μM phytate-P, or 2000 ​μM PR-P, with 200 ​μM soluble-P as a sufficient P control. P. vittata efficiently acquired P when growing under all three low-P sources, with 76–85% greater P in its biomass compared to the sufficient P control. To acquire P from insoluble source, P. vittata secreted 1.7−2.9 fold more organic acids, including malic acid, succinic acid, oxalic acid, and phytic acid as root exudates under phytate and PR treatments. Further, P. vittata increased phytase activity to hydrolyze phytate, showing 6.5- and 3.3-fold greater phytase activity in P. vittata roots and root exudates under phytate treatment. Besides, the frond As content rose by 275–384% when growing under three low-P conditions, possibly attributing to 1.2−5.6 fold upregulation of P-transporters PvPht1;3/1;4 in P. vittata roots. Overall, this study suggests that the effective P and As accumulation by P. vittata under P-limiting conditions is associated with its increased root exudation of organic acids and phytase, and the upregulation of its P-transporters. These findings help to enhance the effectiveness of P. vittata in phytoremediation of As-contaminated soil and improve soil P utilization by crop plants.
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spelling doaj-art-c0181f025e7f4e50807997969adda1032025-08-20T03:27:52ZengElsevierSoil & Environmental Health2949-91942025-07-013310015810.1016/j.seh.2025.100158Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rockChun-Yan Hu0Shufen Xiao1Daniel Menezes-Blackburn2Benjamin L. Turner3Yue Cao4Chenjing Liu5Lena Q. Ma6Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, and State Key Laboratory of Soil Pollution Control and Safety, Zhejiang University, Hangzhou, 310058, Zhejiang, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, and State Key Laboratory of Soil Pollution Control and Safety, Zhejiang University, Hangzhou, 310058, Zhejiang, ChinaDepartment of Soils, Water and Agricultural Engineering, Sultan Qaboos University, 123, Muscat, OmanInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, and State Key Laboratory of Soil Pollution Control and Safety, Zhejiang University, Hangzhou, 310058, Zhejiang, China; Institute of Agriculture and Life Sciences, Gyeongsang National University, Jinju, 52828, Republic of KoreaSchool of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou, 510006, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, and State Key Laboratory of Soil Pollution Control and Safety, Zhejiang University, Hangzhou, 310058, Zhejiang, China; Corresponding author.Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, and State Key Laboratory of Soil Pollution Control and Safety, Zhejiang University, Hangzhou, 310058, Zhejiang, China; Corresponding author.Phosphorus (P) is an essential macronutrient for plant growth, but its availability in soil is often insufficient to achieve optimum crop yield. The As-hyperaccumulator Pteris vittata thrives under low-P condition, with the underlying mechanisms remaining unclear. To understand the P-scavenging traits of P. vittata, we grew P vittata under three P-limiting conditions, low soluble-P, calcium phytate (insoluble organic P), and phosphate rock (PR; insoluble inorganic P), to quantify plant growth, As and P uptake, root exudates, and the gene expression of P transporters. Plants were grown under hydroponics with 50 ​μM As and 20 ​μM soluble-P, 2000 ​μM phytate-P, or 2000 ​μM PR-P, with 200 ​μM soluble-P as a sufficient P control. P. vittata efficiently acquired P when growing under all three low-P sources, with 76–85% greater P in its biomass compared to the sufficient P control. To acquire P from insoluble source, P. vittata secreted 1.7−2.9 fold more organic acids, including malic acid, succinic acid, oxalic acid, and phytic acid as root exudates under phytate and PR treatments. Further, P. vittata increased phytase activity to hydrolyze phytate, showing 6.5- and 3.3-fold greater phytase activity in P. vittata roots and root exudates under phytate treatment. Besides, the frond As content rose by 275–384% when growing under three low-P conditions, possibly attributing to 1.2−5.6 fold upregulation of P-transporters PvPht1;3/1;4 in P. vittata roots. Overall, this study suggests that the effective P and As accumulation by P. vittata under P-limiting conditions is associated with its increased root exudation of organic acids and phytase, and the upregulation of its P-transporters. These findings help to enhance the effectiveness of P. vittata in phytoremediation of As-contaminated soil and improve soil P utilization by crop plants.http://www.sciencedirect.com/science/article/pii/S2949919425000317Root exudatesPhytoremediationAs, P and Ca uptakeAs and P competitionOxalic and phytic acidMalic and succinic acid
spellingShingle Chun-Yan Hu
Shufen Xiao
Daniel Menezes-Blackburn
Benjamin L. Turner
Yue Cao
Chenjing Liu
Lena Q. Ma
Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock
Soil & Environmental Health
Root exudates
Phytoremediation
As, P and Ca uptake
As and P competition
Oxalic and phytic acid
Malic and succinic acid
title Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock
title_full Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock
title_fullStr Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock
title_full_unstemmed Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock
title_short Phosphorus limitation enhances plant growth and arsenic accumulation in As-hyperaccumulator Pteris vittata: Insights from insoluble calcium phytate and phosphate rock
title_sort phosphorus limitation enhances plant growth and arsenic accumulation in as hyperaccumulator pteris vittata insights from insoluble calcium phytate and phosphate rock
topic Root exudates
Phytoremediation
As, P and Ca uptake
As and P competition
Oxalic and phytic acid
Malic and succinic acid
url http://www.sciencedirect.com/science/article/pii/S2949919425000317
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