Physiological and molecular responses in phosphorus-hyperaccumulating Polygonum species to high phosphorus exposure.

hyperaccumulator metabolome photosynthesis tolerance transcriptome trehalose

Journal

Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004

Informations de publication

Date de publication:
03 Apr 2024
Historique:
revised: 16 02 2024
received: 05 09 2023
accepted: 11 03 2024
medline: 3 4 2024
pubmed: 3 4 2024
entrez: 3 4 2024
Statut: aheadofprint

Résumé

Phosphorus (P)-hyperaccumulators for phytoextraction from P-polluted areas generally show rapid growth and accumulate large amounts of P without any toxicity symptom, which depends on a range of physiological processes and gene expression patterns that have never been explored. We investigated growth, leaf element concentrations, P fractions, photosynthetic traits, and leaf metabolome and transcriptome response in amphibious P-hyperaccumulators, Polygonum hydropiper and P. lapathifolium, to high-P exposure (5 mmol L

Identifiants

pubmed: 38567814
doi: 10.1111/pce.14895
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Natural Science Foundation of China
ID : 31972499
Organisme : National Natural Science Foundation of China
ID : 32000064
Organisme : Open Project Foundation of State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China
ID : SKL-KF202213
Organisme : Youth Science Foundation of Sichuan Province
ID : 2022NSFSC1664

Informations de copyright

© 2024 John Wiley & Sons Ltd.

Références

Anders, S. & Huber, W. (2012) Differential expression of RNA‐Seq data at the gene level ‐ the DESeq package. Heidelberg, Germany: European Molecular Biology Laboratory.
Arrivault, S., Guenther, M., Ivakov, A., Feil, R., Vosloh, D., van Dongen, J.T. et al. (2009) Use of reverse‐phase liquid chromatography, linked to tandem mass spectrometry, to profile the Calvin cycle and other metabolic intermediates in Arabidopsis rosettes at different carbon dioxide concentrations. The Plant Journal, 59(5), 826–839.
Aziz, T., Lambers, H., Nicol, D. & Ryan, M.H. (2015) Mechanisms for tolerance of very high tissue phosphorus concentrations in Ptilotus polystachyus. Plant, Cell & Environment, 38(4), 790–799.
Baena‐González, E. & Lunn, J.E. (2020) SnRK1 and trehalose 6‐phosphate ‐ two ancient pathways converge to regulate plant metabolism and growth. Current Opinion in Plant Biology, 55, 52–59.
Bauwe, H., Hagemann, M., Kern, R. & Timm, S. (2012) Photorespiration has a dual origin and manifold links to central metabolism. Current Opinion in Plant Biology, 15(3), 269–275.
Beadle, C.L. & Long, S.P. (1985) Photosynthesis ‐ is it limiting to biomass production? Biomass, 8(2), 119–168.
Bhalla, K., Qu, X., Kretschmer, M. & Kronstad, J.W. (2022) The phosphate language of fungi. Trends in Microbiology, 30(4), 338–349.
Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120.
Bracher, A., Whitney, S.M., Hartl, F.U. & Hayer‐Hartl, M. (2017) Biogenesis and metabolic maintenance of Rubisco. Annual Review of Plant Biology, 68, 29–60.
Cong, W.F., Suriyagoda, L.D.B. & Lambers, H. (2020) Tightening the phosphorus cycle through phosphorus‐efficient crop genotypes. Trends in Plant Science, 25(10), 967–975.
Ding, W., Clode, P.L., Clements, J.C. & Lambers, H. (2018) Sensitivity of different Lupinus species to calcium under a low phosphorus supply. Plant, Cell & Environment, 41(7), 1512–1523.
Ellsworth, D.S., Crous, K.Y., De Kauwe, M.G., Verryckt, L.T., Goll, D., Zaehle, S. et al. (2022) Convergence in phosphorus constraints to photosynthesis in forests around the world. Nature Communications, 13(1), 5005.
Fernandez, O., Béthencourt, L., Quero, A., Sangwan, R.S., & Clément, C. (2010) Trehalose and plant stress responses: friend or foe? Trends in Plant Science, 15(7), 409–417.
Fischer, P., Pöthig, R. & Venohr, M. (2017) The degree of phosphorus saturation of agricultural soils in Germany: current and future risk of diffuse P loss and implications for soil P management in Europe. Science of the Total Environment, 599‐600, 1130–1139.
Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I. et al. (2011) Full‐length transcriptome assembly from RNA‐Seq data without a reference genome. Nature Biotechnology, 29(7), 644–652.
Gupta, R., Walvekar, A.S., Liang, S., Rashida, Z., Shah, P. & Laxman, S. (2019) A tRNA modification balances carbon and nitrogen metabolism by regulating phosphate homeostasis. eLife, 8, e44795.
Hawkins, H.J., Hettasch, H., Mesjasz‐Przybylowicz, J., Przybylowicz, W. & Cramer, M.D. (2008) Phosphorus toxicity in the Proteaceae: a problem in post‐agricultural lands. Scientia Horticulturae, 117(4), 357–365.
Hayes, P.E., Guilherme Pereira, C., Clode, P.L. & Lambers, H. (2019) Calcium‐enhanced phosphorus toxicity in calcifuge and soil‐indifferent Proteaceae along the Jurien Bay chronosequence. New Phytologist, 221(2), 764–777.
Hu, B., Jiang, Z., Wang, W., Qiu, Y., Zhang, Z., Liu, Y. et al. (2019) Nitrate‐NRT1.1B‐SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nature Plants, 5(4), 401–413.
Hussein, S., EL‐Magly, U., Tantawy, M., Kawashty, S. & Saleh, N. (2017) Phenolics of selected species of Persicaria and Polygonum (Polygonaceae) in Egypt. Arabian Journal of Chemistry, 10, 76–81.
Jaffré, T., Brooks, R.R., Lee, J. & Reeves, R.D. (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science, 193(4253), 579–580.
Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M. et al. (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Research, 36, D480–D484.
Lam, K.L., Solon, K., Jia, M., Volcke, E.I.P. & van der Hoek, J.P. (2022) Life cycle environmental impacts of wastewater‐derived phosphorus products: an agricultural end‐user perspective. Environmental Science & Technology, 56(14), 10289–10298.
Lambers, H. (2022) Phosphorus acquisition and utilization in plants. Annual Review of Plant Biology, 73, 17–42.
Lambers, H., Cawthray, G.R., Giavalisco, P., Kuo, J., Laliberté, E., Pearse, S.J. et al. (2012) Proteaceae from severely phosphorus‐impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus‐use‐efficiency. New Phytologist, 196(4), 1098–1108.
Li, Y., Lin, J., Huang, Y., Yao, Y., Wang, X., Liu, C. et al. (2020) Bioaugmentation‐assisted phytoremediation of manganese and cadmium co‐contaminated soil by Polygonaceae plants (Polygonum hydropiper L. and Polygonum lapathifolium L.) and Enterobacter sp. FM‐1. Plant and Soil, 448(1), 439–453.
Li, Z., Hu, J., Wu, Y., Wang, J., Song, H., Chai, M. et al. (2022) Integrative analysis of the metabolome and transcriptome reveal the phosphate deficiency response pathways of alfalfa. Plant Physiology and Biochemistry, 170, 49–63.
Ljungdahl, P.O. & Daignan‐Fornier, B. (2012) Regulation of amino acid, nucleotide, and phosphate metabolism in Saccharomyces cerevisiae. Genetics, 190(3), 885–929.
Long, S.P., Marshall‐Colon, A. & Zhu, X.G. (2015) Meeting the global food demand of the future by engineering crop photosynthesis and yield potential. Cell, 161(1), 56–66.
Long, S.P., Zhu, X.G., Naidu, S.L. & Ort, D.R. (2006) Can improvement in photosynthesis increase crop yields? Plant, Cell & Environment, 29(3), 315–330.
Lu, R.K. (1999) Analysis of soil agrochemistry. Beijing, China: Chinese Agricultural Science and Technology Press.
Luo, B., Ma, P., Nie, Z., Zhang, X., He, X., Ding, X. et al. (2019) Metabolite profiling and genome‐wide association studies reveal response mechanisms of phosphorus deficiency in maize seedling. The Plant Journal, 97(5), 947–969.
Manara, A., Fasani, E., Furini, A. & DalCorso, G. (2020) Evolution of the metal hyperaccumulation and hypertolerance traits. Plant, Cell & Environment, 43(12), 2969–2986.
Meitzel, T., Radchuk, R., McAdam, E.L., Thormählen, I., Feil, R., Munz, E. et al. (2021) Trehalose 6‐phosphate promotes seed filling by activating auxin biosynthesis. New Phytologist, 229(3), 1553–1565.
Mostofa, M.G., Hossain, M.A. & Fujita, M. (2015) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co‐induction of antioxidant defense and glyoxalase systems. Protoplasma, 252(2), 461–475.
Müller, J., Gödde, V., Niehaus, K. & Zörb, C. (2015) Metabolic adaptations of white lupin roots and shoots under phosphorus deficiency. Frontiers in Plant Science, 6, 1014.
Raines, C.A. (2011) Increasing photosynthetic carbon assimilation in C3 plants to improve crop yield: current and future strategies. Plant Physiology, 155(1), 36–42.
Roberts, A. & Pachter, L. (2013) Streaming fragment assignment for real‐time analysis of sequencing experiments. Nature Methods, 10(1), 71–73.
Ruan, Y.L. (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology, 65, 33–67.
Ryabova, A., Cornette, R., Cherkasov, A., Watanabe, M., Okuda, T., Shagimardanova, E. et al. (2020) Combined metabolome and transcriptome analysis reveals key components of complete desiccation tolerance in an anhydrobiotic insect. Proceedings of the National Academy of Sciences of the United States of America, 117(32), 19209–19220.
Ryan, M.H., Ehrenberg, S., Bennett, R.G. & Tibbett, M. (2009) Putting the P in Ptilotus: a phosphorus‐accumulating herb native to Australia. Annals of Botany, 103(6), 901–911.
Ryan, M.H., Kaur, P., Nazeri, N.K., Clode, P.L., Keeble‐Gagnère, G., Doolette, A.L. et al. (2019) Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition. Plant, Cell & Environment, 42, 1987–2002.
Schelske, C.L. (2009) Eutrophication: focus on phosphorus. Science, 324(5928), 722.
Schindler, D.W., Carpenter, S.R., Chapra, S.C., Hecky, R.E. & Orihel, D.M. (2016) Reducing phosphorus to curb lake eutrophication is a success. Environmental Science & Technology, 50(17), 8923–8929.
Schluepmann, H., Berke, L. & Sanchez‐Perez, G.F. (2012) Metabolism control over growth: a case for trehalose‐6‐phosphate in plants. Journal of Experimental Botany, 63(9), 3379–3390.
Seimandi, G., Álvarez, N., Stegmayer, M.I., Fernández, L., Ruiz, V., Favaro, M.A. et al. (2021) An update on phytochemicals and pharmacological activities of the genus Persicaria and Polygonum. Molecules, 26(19), 5956.
Sharma, N.C. & Sahi, S.V. (2011) Enhanced organic phosphorus assimilation promoting biomass and shoot P hyperaccumulations in Lolium multiflorum grown under sterile conditions. Environmental Science & Technology, 45(24), 10531–10537.
Sulpice, R., Ishihara, H., Schlereth, A., Cawthray, G.R., Encke, B., Giavalisco, P. et al. (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus‐use efficiency of Proteaceae species. Plant, Cell & Environment, 37(6), 1276–1298.
Suriyagoda, L.D.B., Ryan, M.H., Gille, C.E., Dayrell, R.L.C., Finnegan, P.M., Ranathunge, K. et al. (2023) Phosphorus fractions in leaves. New Phytologist, 237(4), 1122–1135.
Takagi, D., Miyagi, A., Tazoe, Y., Suganami, M., Kawai‐Yamada, M., Ueda, A. et al. (2020) Phosphorus toxicity disrupts Rubisco activation and reactive oxygen species defence systems by phytic acid accumulation in leaves. Plant, Cell & Environment, 43(9), 2033–2053.
Thomas, D.S., Montagu, K.D. & Conroy, J.P. (2006) Leaf inorganic phosphorus as a potential indicator of phosphorus status, photosynthesis and growth of Eucalyptus grandis seedlings. Forest Ecology and Management, 223(1–3), 267–274.
Veneklaas, E.J., Lambers, H., Bragg, J., Finnegan, P.M., Lovelock, C.E., Plaxton, W.C. et al. (2012) Opportunities for improving phosphorus‐use efficiency in crop plants. New Phytologist, 195(2), 306–320.
Voss, I., Sunil, B., Scheibe, R. & Raghavendra, A.S. (2013) Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biology, 15(4), 713–722.
Wang, D., Gan, X., Wang, Z., Jiang, S., Zheng, X., Zhao, M. et al. (2023) Research status on remediation of eutrophic water by submerged macrophytes: a review. Process Safety and Environmental Protection, 169, 671–684.
Wang, J.C., Chen, X.F., Chu, S.H., You, Y.M., Chi, Y.W., Wang, R.Y. et al. (2022a) Comparative cytology combined with transcriptomic and metabolomic analyses of Solanum nigrum L. in response to Cd toxicity. Journal of Hazardous Materials, 423, 127168.
Wang, X., Wei, C.X., He, F. & Yang, Q.C. (2022b) MtPT5 phosphate transporter is involved in leaf growth and phosphate accumulation of Medicago truncatula. Frontiers of Plant Science, 13, 1005895.
Wang, Y.L., Lysøe, E., Armarego‐Marriott, T., Erban, A., Paruch, L., van Eerde, A. et al. (2018) Transcriptome and metabolome analysis provide insights into root and root released organic anion responses to phosphorus deficiency in oat. Journal of Experimental Botany, 69(15), 3759–3771.
Xiao, G., Li, T., Zhang, X., Yu, H., Huang, H. & Gupta, D.K. (2009) Uptake and accumulation of phosphorus by dominant plant species growing in a phosphorus mining area. Journal of Hazardous Materials, 171(1–3), 542–550.
Xu, W., Zhang, Q., Yuan, W., Xu, F., Muhammad Aslam, M., Miao, R. et al. (2020) The genome evolution and low‐phosphorus adaptation in white lupin. Nature Communications, 11(1), 1069.
Yadav, U.P., Ivakov, A., Feil, R., Duan, G.Y., Walther, D., Giavalisco, P. et al. (2014) The sucrose‐trehalose 6‐phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. Journal of Experimental Botany, 65(4), 1051–1068.
Yan, L., Zhang, X., Han, Z., Pang, J., Lambers, H. & Finnegan, P.M. (2019) Responses of foliar phosphorus fractions to soil age are diverse along a 2 Myr dune chronosequence. New Phytologist, 223(3), 1621–1633.
Ye, D., Clode, P.L., Hammer, T.A., Pang, J., Lambers, H. & Ryan, M.H. (2021) Accumulation of phosphorus and calcium in different cells protects the phosphorus‐hyperaccumulator Ptilotus exaltatus from phosphorus toxicity in high‐phosphorus soils. Chemosphere, 264, 128438.
Ye, D., Li, T., Chen, G., Zheng, Z., Yu, H. & Zhang, X. (2014) Influence of swine manure on growth, P uptake and activities of acid phosphatase and phytase of Polygonum hydropiper. Chemosphere, 105, 139–145.
Ye, D., Li, T., Zhang, X. & Zheng, Z. (2018) Subcellular distribution and chemical form of phosphorus involved in alleviating phosphorus toxicity of the phosphorus‐accumulator Polygonum hydropiper. Chemosphere, 194, 570–578.
Ye, D., Li, T., Zhang, X., Zheng, Z. & Dai, W. (2017) Rhizosphere P composition, phosphatase and phytase activities of Polygonum hydropiper grown in excess P soils. Biology and Fertility of Soils, 53(8), 823–836.
Ye, D., Xie, M., Zhang, X., Huang, H., Yu, H., Zheng, Z. et al. (2022) Evaluation for phosphorus accumulation and removal capability of nine species in the Polygonaceae to excavate amphibious superstars used for phosphorus‐phytoextraction. Chemosphere, 308, 136361.
Yu, G., Ullah, H., Wang, X., Liu, J., Chen, B., Jiang, P. et al. (2023) Integrated transcriptome and metabolome analysis reveals the mechanism of tolerance to manganese and cadmium toxicity in the Mn/Cd hyperaccumulator Celosia argentea Linn. Journal of Hazardous Materials, 443, 130206.
Yu, Q., Ni, X., Cheng, X., Ma, S., Tian, D., Zhu, B. et al. (2022) Foliar phosphorus allocation and photosynthesis reveal plants' adaptative strategies to phosphorus limitation in tropical forests at different successional stages. The Science of the Total Environment, 846, 157456.
Zhang, Y., Lai, J.L., Ji, X.H. & Luo, X.G. (2020) Unraveling response mechanism of photosynthetic metabolism and respiratory metabolism to uranium‐exposure in Vicia faba. Journal of Hazardous Materials, 398, 122997.
Zhao, H., Su, T., Huo, L., Wei, H., Jiang, Y., Xu, L. et al. (2015) Unveiling the mechanism of melatonin impacts on maize seedling growth: sugar metabolism as a case. Journal of Pineal Research, 59(2), 255–266.

Auteurs

Daihua Ye (D)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.
State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, Sichuan, China.

Min Xie (M)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Tao Liu (T)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Huagang Huang (H)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Xizhou Zhang (X)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Haiying Yu (H)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Zicheng Zheng (Z)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Yongdong Wang (Y)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Yu Tang (Y)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Tingxuan Li (T)

College of Resources, Sichuan Agricultural University, Chengdu, Sichuan, China.

Classifications MeSH