High-level expression of a novel chromoplast phosphate transporter ClPHT4;2 is required for flesh color development in watermelon

New Phytologist

Volumn 213, Issue 3, 2017, Pages 1208-1221

  Zhang, Jie ^a   Guo, Shaogui ^a   Ren, Yi ^a   Zhang, Haiying ^a   Gong, Guoyi ^a   Zhou, Ming ^a   Wang, Guizhang ^a   Zong, Mei ^a   He, Hongju ^a   Liu, Fan ^a   Xu, Yong ^a  

^a BEIJING VEGETABLE RESEARCH CENTER   (China)

Author keywords

chromoplast; Citrullus lanatus; flesh color; phosphate transporter; transcriptional regulation

Indexed keywords

CAROTENOID; COLOR; CULTIVAR; DEVELOPMENTAL BIOLOGY; DICOTYLEDON; GENE EXPRESSION; MOLECULAR ANALYSIS; MUTATION; SUGAR; YEAST;

CITRULLUS LANATUS; CITRULLUS LANATUS VAR. LANATUS;

ABSCISIC ACID; AMINOETHOXYVINYLGLYCINE; CAROTENOID; ETHEPHON; FLURIDONE; GLUCOSE; GLYCINE; MESSENGER RNA; ORGANOPHOSPHORUS COMPOUND; PHOSPHATE TRANSPORTER; PLANT PROTEIN; PROTEIN BINDING; PYRIDONE DERIVATIVE; SUCROSE; TRANSCRIPTION FACTOR;

ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CELL FRACTIONATION; CITRULLUS; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; ECOTYPE; FRUIT; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PIGMENTATION; PLANT GENE; PLASTID; PROMOTER REGION; TRANSGENIC PLANT; ULTRASTRUCTURE;

ABSCISIC ACID; CAROTENOIDS; CITRULLUS; ECOTYPE; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC COMPLEMENTATION TEST; GLUCOSE; GLYCINE; MUTATION; ORGANOPHOSPHORUS COMPOUNDS; PHENOTYPE; PHOSPHATE TRANSPORT PROTEINS; PIGMENTATION; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PYRIDONES; RESPONSE ELEMENTS; RNA, MESSENGER; SUBCELLULAR FRACTIONS; SUCROSE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85000607361     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14257     Document Type: Article

References (60)

1. Bang H, Davis AR, Kim S, Leskovar DI, King SR. 2010. Flesh color inheritance and gene interactions among canary yellow, pale yellow, and red watermelon. Journal of the American Society for Horticultural Science 135: 362–368.
2. Bang H, Kim S, Leskovar D, King S. 2007. Development of a codominant CAPS marker for allelic selection between canary yellow and red watermelon based on SNP in lycopene β-cyclase (LCYB) gene. Molecular Breeding 20: 63–72.
3. Bangalore DV, Mcglynn WG, Scott DD. 2008. Effects of fruit maturity on watermelon ultrastructure and intracellular lycopene distribution. Journal of Food Science 73: S222–S228.
4. Bun-Ya M, Nishimura M, Harashima S, Oshima Y. 1991. The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter. Molecular and Cellular Biology 11: 3229–3238.
5. Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J et al. 2011. The basic Helix-Loop-Helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23: 3335–3352.
6. Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M et al. 2002. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14: 2723–2743.
7. Chomicki G, Renner SS. 2015. Watermelon origin solved with molecular phylogenetics including Linnaean material: another example of museomics. New Phytologist 205: 526–532.
8. Collins JK, Perkins-Veazie P, Roberts W. 2006. Lycopene: from plants to humans. HortScience 41: 135–1144.
9. Edwards AJ, Vinyard BT, Wiley ER, Brown ED, Collins JK, Perkins-Veazie P, Baker RA, Clevidence BA. 2003. Consumption of watermelon juice increases plasma concentrations of lycopene and β-carotene in humans. Journal of Nutrition 133: 1043–1050.
10. Egea I, Barsan C, Bian W, Purgatto E, Latché A, Chervin C, Bouzayen M, Pech JC. 2010. Chromoplast differentiation: current status and perspectives. Plant and Cell Physiology 51: 1601–1611.
11. Fischer K. 2011. The import and export business in plastids: transport processes across the inner envelope membrane. Plant Physiology 155: 1511–1519.
12. Flügge UI, Häusler RE, Ludewig F, Gierth M. 2011. The role of transporters in supplying energy to plant plastids. Journal of Experimental Botany 62: 2381–2392.
13. Francesconi M, Lehner B. 2014. The effects of genetic variation on gene expression dynamics during development. Nature 505: 208–211.
14. Göring HH, Curran JE, Johnson MP, Dyer TD, Charlesworth J, Cole SA, Jowett JB, Abraham LJ, Rainwater DL, Comuzzie AG et al. 2007. Discovery of expression QTLs using large-scale transcriptional profiling in human lymphocytes. Nature Genetics 39: 1208–1216.
15. Grassi S, Piro G, Lee JM, Zheng Y, Fei Z, Dalessandro G, Giovannoni JJ, Lenucci MS. 2013. Comparative genomics reveals candidate carotenoid pathway regulators of ripening watermelon fruit. BMC Genomics 14: 781.
16. Guo B, Jin Y, Wussler C, Blancaflor E, Motes C, Versaw WK. 2008. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytologist 177: 889–898.
17. Guo S, Liu J, Zheng Y, Huang M, Zhang H, Gong G, He H, Ren Y, Zhong S, Fei Z et al. 2011. Characterization of transcriptome dynamics during watermelon fruit development: sequencing, assembly, annotation and gene expression profiles. BMC Genomics 12: 454.
18. Guo S, Sun H, Zhang H, Liu J, Ren Y, Gong G, Jiao C, Zheng Y, Yang W, Fei Z et al. 2015. Comparative transcriptiome analysis of cultivated and wild watermelon during fruit development. PLoS One 10: e0130267.
19. Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z et al. 2013. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genetics 45: 51–58.
20. Henderson WR, Scott GH, Wehner TC. 1998. Interaction of flesh color genes in watermelon. Journal of Heredity 89: 50–53.
21. Irigoyen S, Karlsson PM, Kuruvilla J, Spetea C, Versaw WK. 2011. The sink-specific plastidic phosphate transporter PHT4;2 influences starch accumulation and leaf size in Arabidopsis. Plant Physiology 157: 1765–1777.
22. Jeffery J, Holzenburg A, Kin S. 2012. Physical barriers to carotenoid bioaccessibility. Ultrastructure survey of chromoplast and cell wall morphology in nine carotenoid-containing fruits and vegetables. Journal of the Science of Food and Agriculture 92: 2594–2602.
23. Jeffrey C. 2001. Cucurbitaceae. In: Hanelt P, ed. Mansfeld's encyclopedia of agricultural and horticultural crops 3. Berlin, Germany: Springer-Verlag, 1510–1557.
24. Kang BS, Zhao W, Hou YB, Tian P. 2010. Expression of carotenogenic genes during the development and ripening of watermelon fruit. Scientia Horticulture 124: 368–375.
25. Karakurt Y, Huber D. 2002. Cell wall-degrading enzymes and pectin solubility and depolymerization in immature and ripe watermelon (Citrullus lanatus) fruit in response to exogenous ethylene. Physiologia Plantarum 116: 398–405.
26. Koch KE. 1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 509–540.
27. Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK. 2012. Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Molecular Genetics and Genomics 287: 189–203.
28. Lee JM, Joung JG, McQuinn R, Chung MY, Fei Z, Tieman D, Klee H, Giovannoni J. 2012. Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethyleneresponse factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant Journal 70: 191–204.
29. Li L, Yuan H. 2013. Chromoplast biogenesis and carotenoid accumulation. Archives of Biochemistry and Biophysics 539: 102–109.
30. Lin CY, Ku HM, Chiang YH, Ho HY, Yu TA, Jan FJ. 2012. Development of transgenic watermelon resistant to Cucumber mosaic virus and Watermelon mosaic virus by using a single chimeric transgene construct. Transgenic Research 21: 983–993.
31. Liu TY, Huang TK, Yang SY, Hong YT, Huang SM, Wang FN, Chiang SF, Tsai SY, Lu WC, Chiou TJ. 2016. Identification of plant vacuolar transporters mediating phosphate storage. Nature Communications 7: 11095.
32. Liu M, Pirrello J, Chervin C, Roustan JP, Bouzayen M. 2015. Ethylene control of fruit ripening: revisiting the complex network of transcriptional regulation. Plant Physiology 169: 2380–2390.
33. Loqué D, Lalonde S, Looger LL, von Wiren N, Frommer WB. 2007. A cytosolic trans-activation domain essential for ammonium uptake. Nature 446: 195–198.
34. Naz A, Butt MS, Sultan MT, Qayyum MM, Niaz RS. 2014. Watermelon lycopene and allied health claims. Excli Journal 13: 650–660.
35. Nisar N, Li L, Lu S, Khin NC, Pogson BJ. 2015. Carotenoid metabolism in plants. Molecular Plant 8: 68–82.
36. Paris HS. 2015. Origin and emergence of the sweet dessert watermelon, Citrullus lanatus. Annals of Botany 116: 133–148.
37. Pateraki I, Renato M, Azcón-Bieto J, Boronat A. 2013. An ATP synthaseharboring an atypical g-subunit is involved in ATP synthesis in tomato fruit chromoplasts. Plant Journal 74: 74–85.
38. +-dependent phosphate transporter functional characterization in Escherichia coli. Journal of Biological Chemistry 283: 13520–13527.
39. Quick WP, Neuhaus HE. 1996. Evidence for two types of phosphate translocators in sweet-pepper (Capsicum annuum L.) fruit chromoplasts. Biochemical Journal 320: 7–10.
40. Rausch C, Bucher M. 2002. Molecular mechanisms of phosphate transport in plants. Planta 216: 23–37.
41. Ren Y, McGregor C, Zhang Y, Gong G, Zhang H, Guo S, Sun H, Cai W, Zhang J, Xu Y. 2014. An integrated genetic map based on four mapping populations and quantitative trait loci associated with economically important traits in watermelon (Citrullus lanatus). BMC Plant Biology 14: 33.
42. Renato M, Pateraki I, Boronat A, Azcón-Bieto J. 2014. Tomato fruit chromoplasts behave as respiratory bioenergetic organelles during ripening. Plant Physiology 166: 920–933.
43. Rolland F, Baena-Gonzalez E, Sheen J. 2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57: 675–709.
44. Rombauts S, Dehais P, Van Montagu M, Rouze P. 1999. PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Research 27: 295–296.
45. Ruan YL. 2014. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology 65: 33–67.
46. Sarkar AK, Lahiri A. 2013. Specificity determinants for the abscisic acid response element. FEBS Open Bio 3: 101–105.
47. Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C. 2013. Fruit development and ripening. Annual Review of Plant Biology 64: 219–241.
48. Smeekens S, Ma J, Hanson J, Rolland F. 2010. Sugar signals and molecular networks controlling plant growth. Current Opinion in Plant Biology 13: 274–279.
49. Su L, Diretto G, Purgatto E, Danoun S, Zouine M, Li Z, Roustan JP, Bouzayen M, Giuliano G, Chervin C. 2015. Carotenoid accumulation during tomato fruit ripening is modulated by the auxin-ethylene balance. BMC Plant Biology 15: 114.
50. Wang YQ, Yang Y, Fei Z, Yuan H, Fish T, Thannhauser TW, Mazourek M, Kochian LV, Wang X, Li L. 2013. Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. Journal of Experimental Botany 64: 949–961.
51. Welsch R, Maass D, Voegel T, Dellapenna D, Beyer P. 2007. Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiology 145: 1073–1085.
52. Welsch R, Medina J, Giuliano G, Beyer P, von Lintig J. 2003. Structural and functional characterization of the phytoene synthase promoter from Arabidopsis. Planta 216: 523–534.
53. Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Schütze K, Wang X, Chaban C, Hanson J, Teige M, Harter K et al. 2009. Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant Molecular Biology 69: 107–119.
54. Wen L, Li Y. 2009. Distribution of an ankyrin-repeat protein on the endoplasmic reticulum in Arabidopsis. Journal of Integrative Plant Biology 51: 140–146.
55. Wiese A, Elzinga N, Wobbes B, Smeekens S. 2004. A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16: 1717–1729.
56. Yan X, Wang H, Ye Y, Zeng G, Ma R, Mi F, Yao L. 2012. pYBA100: an ease-of-use binary vector with LoxP-FRT recombinase site for plant transformation. Molecular Plant Breeding 10: 371–379.
57. Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols 2: 1565–1572.
58. Yuan H, Zhang J, Coimbatore D, Li L. 2015. Carotenoid metabolism and regulation in horticultural crops. Horticulture Research 2: 15036.
59. Zhang H, Fan J, Guo S, Ren Y, Gong G, Zhang J, Wen Y, Davis A, Xu Y. 2016. Genetic diversity, population structure, and formation of a core collection of 1197 Citrullus accessions. HortScience 51: 23–29.
60. Zhang J, Gong G, Guo S, Ren Y, Zhang H, Xu Y. 2014. Fine mapping of the flesh color controlling genes in watermelon (Citrullus lanatus). In: Harbor B, ed. Curcurbitaceae 2014 Proceedings, Michigan, USA. Alexandria, VA: American Society for Horticultural Science Press, 111–116.