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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The role of the chloroplast localised phosphate transporter GmPHT4;10 gene in plant growth, photosynthesis and drought resistance

Liwei Liu A , Xu He A , Shuwen Wang A , Xueting Qin A , Songhao Che A , Lei Wu A , Dongchao Wang B , Ping Tian B , Xiaoshuang Wei B , Zhihai Wu B , Xue Yang https://orcid.org/0000-0002-4666-1774 A * and Meiying Yang https://orcid.org/0000-0003-1295-5472 A *
+ Author Affiliations
- Author Affiliations

A College of Life Sciences, Jilin Agricultural University, Changchun, Jilin 130118, China.

B College of Agronomy, Jilin Agricultural University, Changchun, Jilin 130118, China.


Handling Editor: Frans Maathuis

Functional Plant Biology 50(8) 649-662 https://doi.org/10.1071/FP23008
Submitted: 9 January 2023  Accepted: 19 May 2023   Published: 13 June 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

In view of the importance of inorganic phosphate to plant growth and development, the role of phosphate transporters responsible for absorption and transportation in crops has attracted increasing attention. In this study, bioinformatics analysis and subcellular localisation experiment showed that GmPHT4;10 is a member of PHT4 subfamily of phosphate transporters and located in chloroplasts. The gene was induced by phosphate deficiency and drought, and was the highest in leaves. After GmPHT4;10 gene was replenished to AtPHT4;5 gene deletion mutant lines (atpht4;5), the phenotype of the transgenic lines was basically recovered to the level of wild-type, but there were significant differences in phosphate content and photosynthetic indicators between wild-type and revertant lines. Meanwhile, the difference of proline content and catalase activity between the two lines also indicated that GmPHT4;10 gene and its orthologous gene AtPHT4;5 were different in drought resistance and drought resistance mechanism. After overexpression of GmPHT4;10 gene in Arabidopsis thaliana, more phosphate and proline were accumulated in chloroplasts and catalase activity was increased, thus improving photosynthesis and drought resistance of plants. The results further supplement the cognition of PHT4 subfamily function, and provides new ideas and ways to improve photosynthesis by revealing the function of chloroplast phosphate transporter.

Keywords: drought stress, functional differentiation, Glycine max, orthologous gene, phosphate deficiency, phosphate transporter, photosynthesis, transgenic plants.


References

Aslam MM, Waseem M, Weifeng X, Qamar MTu (2022) Identification and expression analysis of phosphate transporter (PHT) gene family in Lupinus albus cluster root under phosphorus stress. International Journal of Biological Macromolecules 205, 772–781.
Identification and expression analysis of phosphate transporter (PHT) gene family in Lupinus albus cluster root under phosphorus stress.Crossref | GoogleScholarGoogle Scholar |

Behnke H-D (1973) Plastids in sieve elements and their companion cells. Planta 110, 321–328.
Plastids in sieve elements and their companion cells.Crossref | GoogleScholarGoogle Scholar |

Behnke HD (1991) Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons. Aliso 13, 167–182.
Distribution and evolution of forms and types of sieve-element plastids in the dicotyledons.Crossref | GoogleScholarGoogle Scholar |

Birchler JA, Yang H (2022) The multiple fates of gene duplications: deletion, hypofunctionalization, subfunctionalization, neofunctionalization, dosage balance constraints, and neutral variation. The Plant Cell 34, 2466–2474.
The multiple fates of gene duplications: deletion, hypofunctionalization, subfunctionalization, neofunctionalization, dosage balance constraints, and neutral variation.Crossref | GoogleScholarGoogle Scholar |

Bucher M, Fabiańska I (2016) Long-sought vacuolar phosphate transporters identified. Trends in Plant Science 21, 463–466.
Long-sought vacuolar phosphate transporters identified.Crossref | GoogleScholarGoogle Scholar |

Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C, Pribil M, Husted S (2018) The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiology 177, 271–284.
The impacts of phosphorus deficiency on the photosynthetic electron transport chain.Crossref | GoogleScholarGoogle Scholar |

Daram P, Brunner S, Rausch C, Steiner C, Amrhein N, Bucher M (1999) Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis. The Plant Cell 11, 2153–2166.
Pht2;1 encodes a low-affinity phosphate transporter from Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Gao JF (2006) ‘Experimental guidance of plant physiology.’ (Higher Education Press: Beijing, China)

Gu M, Chen A, Sun S, Xu G (2016) Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing? Molecular Plant 9, 396–416.
Complex regulation of plant phosphate transporters and the gap between molecular mechanisms and practical application: what is missing?Crossref | GoogleScholarGoogle Scholar |

Guo B, Jin Y, Wussler C, Blancaflor EB, Motes CM, Versaw WK (2008a) Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytologist 177, 889–898.
Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters.Crossref | GoogleScholarGoogle Scholar |

Guo B, Irigoyen S, Fowler TB, Versaw WK (2008b) Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues. Plant Signaling & Behavior 3, 784–790.
Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues.Crossref | GoogleScholarGoogle Scholar |

Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X, Lu W, Xiao K (2013) Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237, 1163–1178.
Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions.Crossref | GoogleScholarGoogle Scholar |

Haferkamp I (2007) The diverse members of the mitochondrial carrier family in plants. FEBS Letters 581, 2375–2379.
The diverse members of the mitochondrial carrier family in plants.Crossref | GoogleScholarGoogle Scholar |

Hilgers EJA, Schöttler MA, Mettler-Altmann T, Krueger S, Dörmann P, Eicks M, Flügge U-I, Häusler RE (2018) The combined loss of triose phosphate and xylulose 5-phosphate/phosphate translocators leads to severe growth retardation and impaired photosynthesis in Arabidopsis thaliana tpt/xpt double mutants. Frontiers in Plant Science 9, 1331
The combined loss of triose phosphate and xylulose 5-phosphate/phosphate translocators leads to severe growth retardation and impaired photosynthesis in Arabidopsis thaliana tpt/xpt double mutants.Crossref | GoogleScholarGoogle Scholar |

Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant, Cell & Environment 30, 310–322.
Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles.Crossref | GoogleScholarGoogle Scholar |

Jiang M, Caldararu S, Zaehle S, Ellsworth DS, Medlyn BE (2019) Towards a more physiological representation of vegetation phosphorus processes in land surface models. New Phytologist 222, 1223–1229.
Towards a more physiological representation of vegetation phosphorus processes in land surface models.Crossref | GoogleScholarGoogle Scholar |

Li LH, Guo N, Wu ZY, Zhao JM, Sun JT, Wang XT, Xing H (2015) P1BS, a conserved motif involved in tolerance to phosphate starvation in soybean. Genetics and Molecular Research 14, 9384–9394.
P1BS, a conserved motif involved in tolerance to phosphate starvation in soybean.Crossref | GoogleScholarGoogle Scholar |

Li R, Wang J, Xu L, Sun M, Yi K, Zhao H (2020) Functional analysis of phosphate transporter OsPHT4 family members in rice. Rice Science 27, 493–503.
Functional analysis of phosphate transporter OsPHT4 family members in rice.Crossref | GoogleScholarGoogle Scholar |

Liu T-Y, Huang T-K, Yang S-Y, Hong Y-T, Huang S-M, Wang F-N, Chiang S-F, Tsai S-Y, Lu W-C, Chiou T-J (2016) Identification of plant vacuolar transporters mediating phosphate storage. Nature Communications 7, 11095
Identification of plant vacuolar transporters mediating phosphate storage.Crossref | GoogleScholarGoogle Scholar |

Liu X-L, Wang L, Wang X-W, Yan Y, Yang X-L, Xie M-Y, Hu Z, Shen X, Ai H, Lin H-H, Xu G-H, Yang J, Sun S-B (2020) Mutation of the chloroplast-localized phosphate transporter OsPHT2;1 reduces flavonoid accumulation and UV tolerance in rice. The Plant Journal 102, 53–67.
Mutation of the chloroplast-localized phosphate transporter OsPHT2;1 reduces flavonoid accumulation and UV tolerance in rice.Crossref | GoogleScholarGoogle Scholar |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |

Miyaji T, Kuromori T, Takeuchi Y, Yamaji N, Yokosho K, Shimazawa A, Sugimoto E, Omote H, Ma JF, Shinozaki K, Moriyama Y (2015) AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis. Nature Communications 6, 5928
AtPHT4;4 is a chloroplast-localized ascorbate transporter in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Młodzińska E, Zboińska M (2016) Phosphate uptake and allocation – a closer look at Arabidopsis thaliana L. and Oryza sativa L. Frontiers in Plant Science 7, 1198
Phosphate uptake and allocation – a closer look at Arabidopsis thaliana L. and Oryza sativa L.Crossref | GoogleScholarGoogle Scholar |

Muchhal US, Raghothama KG (1999) Transcriptional regulation of plant phosphate transporters. Proceedings of the National Academy of Sciences of the United States of America 96, 5868–5872.
Transcriptional regulation of plant phosphate transporters.Crossref | GoogleScholarGoogle Scholar |

Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annual Review of Plant Physiology and Plant Molecular Biology 51, 111–140.
Nonphotosynthetic metabolism in plastids.Crossref | GoogleScholarGoogle Scholar |

Nussaume L, Kanno S, Javot H, Marin E, Nakanishi TM, Thibaud M-C (2011) Phosphate import in plants: focus on the PHT1 transporters. Frontiers in Plant Science 2, 83
Phosphate import in plants: focus on the PHT1 transporters.Crossref | GoogleScholarGoogle Scholar |

O’Brien KP, Westerlund I, Sonnhammer ELL (2004) OrthoDisease: a database of human disease orthologs. Human Mutation 24, 112–119.
OrthoDisease: a database of human disease orthologs.Crossref | GoogleScholarGoogle Scholar |

Orellana A, Moraga C, Araya M, Moreno A (2016) Overview of nucleotide sugar transporter gene family functions across multiple species. Journal of Molecular Biology 428, 3150–3165.
Overview of nucleotide sugar transporter gene family functions across multiple species.Crossref | GoogleScholarGoogle Scholar |

Pan Y, Song Y, Zhao L, Chen P, Bu C, Liu P, Zhang D (2022) The genetic basis of phosphorus utilization efficiency in plants provide new insight into woody perennial plants improvement. International Journal of Molecular Sciences 23, 2353
The genetic basis of phosphorus utilization efficiency in plants provide new insight into woody perennial plants improvement.Crossref | GoogleScholarGoogle Scholar |

Poirier Y, Bucher M (2002) Phosphate transport and homeostasis in Arabidopsis. The Arabidopsis Book 1, e0024
Phosphate transport and homeostasis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Prathap V, Kumar A, Maheshwari C, Tyagi A (2022) Phosphorus homeostasis: acquisition, sensing, and long-distance signaling in plants. Molecular Biology Reports 49, 8071–8086.
Phosphorus homeostasis: acquisition, sensing, and long-distance signaling in plants.Crossref | GoogleScholarGoogle Scholar |

Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216, 23–37.
Molecular mechanisms of phosphate transport in plants.Crossref | GoogleScholarGoogle Scholar |

Rausch C, Zimmermann P, Amrhein N, Bucher M (2004) Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis. The Plant Journal 39, 13–28.
Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Shi S, Wang D, Yan Y, Zhang F, Wang H, Gu M, Sun S, Xu G (2013) Function of phosphate transporter OsPHT2;1 in improving phosphate utilization in rice. Chinese Journal of Rice Science 27, 457–465.

Stefanovic A, Arpat AB, Bligny R, Gout E, Vidoudez C, Bensimon M, Poirier Y (2011) Over-expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux. The Plant Journal 66, 689–699.
Over-expression of PHO1 in Arabidopsis leaves reveals its role in mediating phosphate efflux.Crossref | GoogleScholarGoogle Scholar |

Tariq A, Pan K, Olatunji OA, Graciano C, Li Z, Sun F, Zhang L, Wu X, Chen W, Song D, Huang D, Xue T, Zhang A (2018) Phosphorous fertilization alleviates drought effects on Alnus cremastogyne by regulating its antioxidant and osmotic potential. Scientific Reports 8, 5644
Phosphorous fertilization alleviates drought effects on Alnus cremastogyne by regulating its antioxidant and osmotic potential.Crossref | GoogleScholarGoogle Scholar |

Tariq A, Pan K, Olatunji OA, Graciano C, Li Z, Li N, Song D, Sun F, Wu X, Dakhil MA, Sun X, Zhang L (2019) Impact of phosphorus application on drought resistant responses of Eucalyptus grandis seedlings. Physiologia Plantarum 166, 894–908.
Impact of phosphorus application on drought resistant responses of Eucalyptus grandis seedlings.Crossref | GoogleScholarGoogle Scholar |

Tominaga J, Shimada H, Kawamitsu Y (2018) Direct measurement of intercellular CO2 concentration in a gas-exchange system resolves overestimation using the standard method. Journal of Experimental Botany 69, 1981–1991.
Direct measurement of intercellular CO2 concentration in a gas-exchange system resolves overestimation using the standard method.Crossref | GoogleScholarGoogle Scholar |

Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible W-R, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306–320.
Opportunities for improving phosphorus-use efficiency in crop plants.Crossref | GoogleScholarGoogle Scholar |

Versaw WK, Harrison MJ (2002) A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. The Plant Cell 14, 1751–1766.
A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses.Crossref | GoogleScholarGoogle Scholar |

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiology 135, 400–411.
Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis.Crossref | GoogleScholarGoogle Scholar |

Wang G-Y, Shi J-L, Ng G, Battle SL, Zhang C, Lu H (2011) Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense. Molecular Plant 4, 516–526.
Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis defense.Crossref | GoogleScholarGoogle Scholar |

Wang D, Lv S, Jiang P, Li Y (2017) Roles, regulation, and agricultural application of plant phosphate transporters. Frontiers in Plant Science 8, 817
Roles, regulation, and agricultural application of plant phosphate transporters.Crossref | GoogleScholarGoogle Scholar |

Wang F, Deng M, Xu J, Zhu X, Mao C (2018) Molecular mechanisms of phosphate transport and signaling in higher plants. Seminars in Cell & Developmental Biology 74, 114–122.
Molecular mechanisms of phosphate transport and signaling in higher plants.Crossref | GoogleScholarGoogle Scholar |

Wu MC, Xiao CZ, Zheng PY (1999) Study on the physilogical function of phosphorus to soybean. Scientia Agricultura Sinica 32, 59–65.

Xue L, Huang X, Zhang Z, Lin Q, Zhong Q, Zhao Y, Gao Z, Xu C (2022) An anthocyanin-related glutathione S-transferase, MrGST1, plays an essential role in fruit coloration in Chinese bayberry (Morella rubra). Frontiers in Plant Science 13, 903333
An anthocyanin-related glutathione S-transferase, MrGST1, plays an essential role in fruit coloration in Chinese bayberry (Morella rubra).Crossref | GoogleScholarGoogle Scholar |

Zhang Z, Ma Z, Chao S, Pang S (1986) The relationship between net photosynthetic rate and yield formation in soybean. Acta Agronomica Sinica 000, 43–48.

Zhang C, Meng S, Li M, Zhao Z (2016) Genomic identification and expression analysis of the phosphate transporter gene family in poplar. Frontiers in Plant Science 7, 1398
Genomic identification and expression analysis of the phosphate transporter gene family in poplar.Crossref | GoogleScholarGoogle Scholar |

Zhang L, Song Z, Li F, Li X, Ji H, Yang S (2019) Retracted Article: The specific MYB binding sites bound by TaMYB in the GAPCp2/3 promoters are involved in the drought stress response in wheat. BMC Plant Biology 19, 366
Retracted Article: The specific MYB binding sites bound by TaMYB in the GAPCp2/3 promoters are involved in the drought stress response in wheat.Crossref | GoogleScholarGoogle Scholar |

Zhao L, Versaw WK, Liu J, Harrison MJ (2003) A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope. New Phytologist 157, 291–302.
A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelope.Crossref | GoogleScholarGoogle Scholar |

Zhu G-J, Jiang G-M, Hao N-B, Liu H-Q, Kong Z-H, Du W-G, Man W-Q (2002) Relationship between ecophysiological features and grain yield in different soybean varieties. Acta Botanica Sinica 44, 725–730.