Phosphorus-induced restructuring of the ascorbate–glutathione cycle and lignin biosynthesis alleviates manganese toxicity in peach roots

Author:

Noor Iqra123,Sohail Hamza123,Wentao Cao12,Zhu Kaijie12,Hasanuzzaman Mirza45,Li Guohuai12,Liu Junwei12ORCID

Affiliation:

1. National Key Lab for Germplasm Innovation and Utilization of Horticultural Crops , College of Horticulture and Forestry Sciences, , No. 1 Shizishan Street, Wuhan 430070, Hubei, PR China

2. Huazhong Agricultural University , College of Horticulture and Forestry Sciences, , No. 1 Shizishan Street, Wuhan 430070, Hubei, PR China

3. School of Horticulture and Landscape Architecture, Yangzhou University , 88 South Daxue road, Yangzhou, 225009, Jiangsu, PR China

4. Department of Agronomy , Faculty of Agriculture, Sher-e-Bangla Nagar, , Sher-e-Bangla Nagar, Dhaka 1207, Bangladesh

5. Sher-e-Bangla Agricultural University , Faculty of Agriculture, Sher-e-Bangla Nagar, , Sher-e-Bangla Nagar, Dhaka 1207, Bangladesh

Abstract

Abstract Manganese (Mn) is indispensable for plant growth, but its excessive uptake in acidic soils leads to toxicity, hampering food safety. Phosphorus (P) application is known to mitigate Mn toxicity, yet the underlying molecular mechanism remains elusive. Here, we conducted physiological and transcriptomic analyses of peach roots response to P supply under Mn toxicity. Manganese treatment disrupted root architecture and caused ultrastructural damage due to oxidative injury. Notably, P application ameliorated the detrimental effects and improved the damaged roots by preventing the shrinkage of cortical cells, epidermis and endodermis, as well as reducing the accumulation of reactive oxygen species (ROS). Transcriptomic analysis revealed the differentially expressed genes enriched in phenylpropanoid biosynthesis, cysteine, methionine and glutathione metabolism under Mn and P treatments. Phosphorus application upregulated the transcripts and activities of core enzymes crucial for lignin biosynthesis, enhancing cell wall integrity. Furthermore, P treatment activated ascorbate–glutathione cycle, augmenting ROS detoxification. Additionally, under Mn toxicity, P application downregulated Mn uptake transporter while enhancing vacuolar sequestration transporter transcripts, reducing Mn uptake and facilitating vacuolar storage. Collectively, P application prevents Mn accumulation in roots by modulating Mn transporters, bolstering lignin biosynthesis and attenuating oxidative stress, thereby improving root growth under Mn toxicity. Our findings provide novel insights into the mechanism of P-mediated alleviation of Mn stress and strategies for managing metal toxicity in peach orchards.

Funder

China Agriculture Research System of MOF and MARA

National Natural Science Foundation of China

National Key Research and Development Program of China

Publisher

Oxford University Press (OUP)

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