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Journal of Integrative Agriculture  2017, Vol. 16 Issue (03): 580-590    DOI: 10.1016/S2095-3119(16)61433-8
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Expression and functional analysis of FaPHO1;H9 gene of strawberry (Fragaria×ananassa)
CAO Fei, LI He, WANG Shou-ming, LI Xiao-ming, DAI Hong-yan, ZHANG Zhi-hong

College of Horticulture, Shenyang Agricultural University, Shenyang 110866, P.R.China

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Abstract  Although the phosphate 1 (PHO1) gene family has been implicated in inorganic phosphate transport and homeostasis, the underlying mechanism of this gene in the strawberry has not yet been revealed.  In the present study, we analyzed the expression of the PHO1;H9 gene in the strawberry (Fragaria×ananassa), revealing the involvement of this gene in the regulation of phosphorus (P) content.  The coding sequence (CDS) of the PHO1;H9 gene, was isolated from the cultivated strawberry ‘Sachinoka’ and named as FaPHO1;H9.  The full-length CDS of this gene was 2 292 bp, encoding 763 amino acids, and the protein contained both SYG1/Pho81/XPR1 (SPX) and ERD1/ XPR1/SYG1 (EXS) domains, which were involved in phosphate (Pi) signaling.  Real-time reverse transcription-polymerase chain reaction (RT-PCR) data suggested that the level of FaPHO1;H9 expression was consistent with the P content in different organs, except for the petiole.  Particularly, its expression level was also correlated with P content in fruits of different developmental stages.  The expression of FaPHO1;H9 was also consistent with P content in leaves under different concentrations of P fertilizer application.  Furthermore, transgenic Arabidopsis lines were generated, and the P content in Arabidopsis plants over-expressing FaPHO1;H9 was significantly higher than that in wild-type plants.  Therefore, we proposed that FaPHO1;H9 functions in P transport.
Keywords:  Fragaria×ananassa      PHO1;H9      phosphorus      expression      fruits      transgenic Arabidopsis
  
Received: 14 March 2016   Accepted:
Fund: 

This work was financially supported by the National Natural Science Foundation of China (31372037) and the Program for Excellent Talents in University of Liaoning Province, China (LJQ2014069).

Corresponding Authors:  ZHANG Zhi-hong, Mobile: +86-13066583902, E-mail: zhang_sau@163.com; LI He, Mobile: +86-13238805558, E-mail: lihe1978721@163.com   
About author:  CAO Fei, E-mail: 15227960912@163.com

Cite this article: 

CAO Fei, LI He, WANG Shou-ming, LI Xiao-ming, DAI Hong-yan, ZHANG Zhi-hong. 2017. Expression and functional analysis of FaPHO1;H9 gene of strawberry (Fragaria×ananassa). Journal of Integrative Agriculture, 16(03): 580-590.

Aaby K, Mazur S, Nes A, Skrede G. 2012. Phenolic compounds in strawberry (Fragaria×ananassa Duch.) fruits: Composition in 27 cultivars and changes during ripening. Food Chemistry, 132, 86–97.
Ames B N. 1966. Assay of inorganic phosphate: total phosphate and phosphatases. Methods in Enzymology, 8, 115–118.
Arpat A B, Magliano P, Wege S, Rouached H, Stefanovic A, Poirier Y. 2012. Functional expression of PHO1 to the Golgi and trans-Golgi network and its role in export of inorganic phosphate. The Plant Journal, 71, 479–491.
Balzergue C, Puech-Pagès V, Bécard G, Rochange S F. 2011. The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. Journal of Experimental Botany, 62, 1049–1060.
Cao F, Guan C Y, Dai H Y, Li X M, Zhang Z H. 2015. Soluble solids content is positively correlated with phosphorus content in ripening strawberry fruits. Scientia Horticulturae, 195, 183–187.
Chen Y F, Li L Q, Xu Q, Kong Y H, Wang H, Wu W H. 2009. The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. The Plant Cell, 21, 3554–3566.
Chiou T J, Lin S I. 2011. Signaling network in sensing phosphate availability in plants. Annual Review of Plant Biology, 62, 185–206.
Clough S J, Bent A F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735–743.
Duan K, Yi K, Dang L, Huang H, Wu W, Wu P. 2008. Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. The Plant Journal, 54, 965–975.
Duncan D B. 1955. Multiple range and multiple F tests. Biometrics, 39, 205–207.
Fait A, Hanhineva K, Beleggia R, Dai N, Rogachev I, Nikiforova V J, Fernie A R, Aharoni A. 2008. Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. The Plant Physiology, 148, 730–750.
Gibson S I. 2005. Control of plant development and gene expression by sugar signaling. Current Opinion in Plant Biology, 8, 93–102.
Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y. 2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. The Plant Cell, 14, 889–902.
Hammond J P, White P J. 2007. Sucrose transport in the phloem: Integrating root responses to phosphorus starvation. Journal of Experimental Botany, 59, 93–109.
He L L, Zhao M, Wang Y, Gai J Y, He C Y. 2013. Phylogeny, structural evolution and functional diversification of the plant PHOSPHATE1 gene family: a focus on Glycine max. BMC Evolutionary Biology, 13, 103.
Hurlimann H C, Pinson B, Stadler-Waibel M, Zeeman S C, Freimoser F M. 2009. The SPX domain of the yeast low-affinity phosphate transporter Pho90 regulates transport activity. EMBO Reports, 10, 1003–1008.
Jia H F, Chai Y M, Li C L, Lu D, Luo J J, Qin L, Shen Y Y. 2011. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiology, 157, 188–199.
Jia H F, Wang Y H, Sun M Z, Li B B, Han Y, Zhao Y X, Li X L, Ding N, Li C, Ji W L, Jia W S. 2013. Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytologist, 198, 453–465.
Karthikeyan A S, Varadarajan D K, Jain A, Held M A, Carpita N C, Raghothama K G. 2007. Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta, 225, 907–918.
Li H, Li T, Fu G, Hu K. 2014. How strawberry plants cope with limited phosphorus supply: Nursery-crop formation and phosphorus and nitrogen uptake dynamics. Journal of Plant Nutrition and Soil Science, 177, 260–270.
Li H, Mao W J, Liu W, Dai H Y, Liu Y X, Ma Y, Zhang Z H. 2013. Deep sequencing discovery of novel and conserved microRNAs in wild type and a white-flesh mutant strawberry. Planta, 238, 695–713.
Liang Y, Li H, Ma Y, Cao F, Dou Y J, Zhang Z H. 2012. Comparative analysis of biological characteristics and quality in a white-flesh strawberry mutant ‘Sachinoka’ and its wild type. Scientia Agricultura Sinica, 45, 3115–3123. (in Chinese)
Lin W Y, Huang T K, Leong S J, Chiou T J. 2014. Long-distance call from phosphate: systemic regulation of phosphate starvation responses. Journal of Experimental Botany, 65, 1817–1827.
Lin W Y, Lin S I, Chiou T J. 2009. Molecular regulators of phosphate homeostasis in plants. Journal of Experimental Botany, 60, 1427–1438.
Liu F, Wang Z, Ren H, Shen C, Li Y, Ling H Q, Wu C, Lian X, Wu P. 2010. OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. The Plant Journal, 62, 508–517.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods, 25, 402–408.
Loreti E, Bellis L D, Alpi A, Perata P. 2001. Why and how do plant cells sense sugars? Annals of Botany, 88, 803–812.
Masny A, Pruski K, Zurawicz E, Madry W. 2016. Breeding value of selected dessert strawberry (Fragaria×ananassa Duch.) cultivars for ripening time, fruit yield and quality. Euphytica, 207, 225–243.
Medeiros R F, Pereira W E, Rodrigues R D, do Nascimento R, Suassuna J F, Dantas T A G. 2015. Growth and yield of strawberry plants fertilized with nitrogen and phosphorus. Revista Brasileira de Engenharia Agrícola e Ambiental, 19, 865–870. (in Portuguese)
Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum, 15, 473–479.
Natr L. 1992. Mineral nutrients-a ubiquitous stress factor for photosynthesis. Photosynthetica, 27, 271–294.
Parsons H T, Christiansen K, Knierim B, Carroll A, Ito J, Batth T S, Smith-Moritz A M, Morrison S, McInerney P, Hadi M Z, Auer M, Mukhopadhyay A, Petzold C J, Scheller H V, Loqué D, Heazlewood J L. 2012. Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiology, 159, 12–26.
Poirier Y, Thoma S, Somerville C, Schiefelbein J. 1991. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiology, 97, 1087–1093.
Rouached H, Arpat A B, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: Signaling players and cross-talks. Molecular Plant, 3, 288–299.
Roussos P A, Denaxa N K, Damvakaris T. 2009. Strawberry fruit quality attributes after application of plant growth stimulating compounds. Scientia Horticulturae, 119, 138–146.
Secco D, Baumann A, Poirier Y. 2010. Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiology, 152, 1693–1704.
Secco D, Wang C, Arpat B A, Wang Z, Poirier Y, Tyerman S D, Wu P, Shou H, Whelan J. 2012. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytologist, 193, 842–851.
Schachtman D P, Shin R. 2007. Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology, 58, 47–69.
Shin H, Shin H S, Dewbre G R, Harrison M J. 2004. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. The Plant Journal, 39, 629–642.
Smeekens S, Ma J, Hanson J, Rolland F. 2000. Sugar signals and molecular networks controlling plant growth. Current Opinion in Plant Biology, 13, 274–279.
Stefanovic A, Arpat A B, 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.
Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, Delessert S, Poirier Y. 2007. Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. The Plant Journal, 50, 982–994.
Ticconi C A, Abel S. 2004. Short on phosphate: Plant surveillance and countermeasures. Trends in Plant Science, 9, 548–555.
Ticconi C A, Delatorre C A, Abel S. 2001. Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiology, 127, 963–972.
Valentinuzzi F, Mason M, Scampicchio M, Andreotti C, Cesco S, Mimmo T. 2015a. Enhancement of the bioactive compound content in strawberry fruits grown under iron and phosphorus deficiency. Journal of the Science of Food and Agriculture, 95, 2088–2094.
Valentinuzzi F, Pii Y, Vigani G, Lehmann M, Cesco S, Mimmo T. 2015b. Phosphorus and iron deficiencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria×ananassa. Journal of Experimental Botany, 66, 6483–6495.
Vance C P, Uhde-Stone C, Allan D L. 2003. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist, 157, 423–447.
Varadarajan D K, Karthikeyan A S, Matilda P D, Raghothama K G. 2002. Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiology, 129, 1232–1240.
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.
Wang Y, Secco D, Poirier Y. 2008. Characterization of the PHO1 gene family and the responses to phosphate deficiency of Physcomitrella patens. Plant Physiology, 146, 646–656.
Wege S, Khan G A, Jung J Y, Vogiatzaki E, Pradervand S, Aller I, Meyer A J, Poirier Y. 2016. The EXS domain of PHO1 participates in the response of shoots to phosphate deficiency via a root-to-shoot signal. Plant Physiology, 170, 385–400.
Wind J, Smeekens S, Hanson J. 2010. Sucrose: metabolite and signaling molecule. Phytochemistry, 71, 1610–1614.
Zhang J J, Wang X, Yu O, Tang J J, Gu X G, Wan X C, Fang C B. 2011. Metabolic profiling of strawberry (Fragaria×ananassa Duch.) during fruit development and maturation. Journal of Experimental Botany, 62, 1103–1118.
Zhang Z, Liao H, Lucas W J. 2014. Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. Journal of Integrative Plant Biology, 56, 192–220.
Zorrilla-Fontanesi Y, Cabeza A, Domínguez P, Medina J J, Valpuesta V, Denoyes-Rothan B, Sánchez-Sevilla J F, Amaya I. 2011. Quantitative trait loci and underlying candidate genes controlling agronomical and fruit quality traits in octoploid strawberry (Fragaria×ananassa). Theoretical and Applied Genetics, 123, 755–778.
 
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