Deciphering the Genomic Structure, Function and Evolution of Carotenogenesis Related Phytoene Synthases in Grasses

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2012 Jun 8

PMID 22672222

Citations 22

Authors

Bianca Dibari

Florent Murat

Audrey Chosson

Veronique Gautier

Charles Poncet

Philippe Lecomte

Ingrid Mercier

Helene Berges

Caroline Pont

Antonio Blanco

Jerome Salse

Affiliations

Soon will be listed here.

Abstract

Background: Carotenoids are isoprenoid pigments, essential for photosynthesis and photoprotection in plants. The enzyme phytoene synthase (PSY) plays an essential role in mediating condensation of two geranylgeranyl diphosphate molecules, the first committed step in carotenogenesis. PSY are nuclear enzymes encoded by a small gene family consisting of three paralogous genes (PSY1-3) that have been widely characterized in rice, maize and sorghum.

Results: In wheat, for which yellow pigment content is extremely important for flour colour, only PSY1 has been extensively studied because of its association with QTLs reported for yellow pigment whereas PSY2 has been partially characterized. Here, we report the isolation of bread wheat PSY3 genes from a Renan BAC library using Brachypodium as a model genome for the Triticeae to develop Conserved Orthologous Set markers prior to gene cloning and sequencing. Wheat PSY3 homoeologous genes were sequenced and annotated, unravelling their novel structure associated with intron-loss events and consequent exonic fusions. A wheat PSY3 promoter region was also investigated for the presence of cis-acting elements involved in the response to abscisic acid (ABA), since carotenoids also play an important role as precursors of signalling molecules devoted to plant development and biotic/abiotic stress responses. Expression of wheat PSYs in leaves and roots was investigated during ABA treatment to confirm the up-regulation of PSY3 during abiotic stress.

Conclusions: We investigated the structural and functional determinisms of PSY genes in wheat. More generally, among eudicots and monocots, the PSY gene family was found to be associated with differences in gene copy numbers, allowing us to propose an evolutionary model for the entire PSY gene family in Grasses.

Citing Articles

SyntenyViewer: a comparative genomics-driven translational research tool.

Flores R, Huneau C, Burlot L, Laine M, Kimmel E, Pommier C Database (Oxford). 2023; 2023.

PMID: 37159239 PMC: 10167986. DOI: 10.1093/database/baad027.

Molecular evolution and diversification of phytoene synthase (PSY) gene family.

Lisboa M, Canal D, Filgueiras J, Turchetto-Zolet A Genet Mol Biol. 2022; 45(4):e20210411.

PMID: 36537743 PMC: 9764326. DOI: 10.1590/1678-4685-GMB-2021-0411.

Phytoene Synthase: The Key Rate-Limiting Enzyme of Carotenoid Biosynthesis in Plants.

Zhou X, Rao S, Wrightstone E, Sun T, Lui A, Welsch R Front Plant Sci. 2022; 13:884720.

PMID: 35498681 PMC: 9039723. DOI: 10.3389/fpls.2022.884720.

Differential Regulation of Phytoene Synthase PSY1 During Fruit Carotenogenesis in Cultivated and Wild Tomato Species ( section Lycopersicon).

Efremov G, Slugina M, Shchennikova A, Kochieva E Plants (Basel). 2020; 9(9).

PMID: 32916928 PMC: 7569967. DOI: 10.3390/plants9091169.

Differential interaction of Or proteins with the PSY enzymes in saffron.

Ahrazem O, Lopez A, Argandona J, Castillo R, Rubio-Moraga A, Gomez-Gomez L Sci Rep. 2020; 10(1):552.

PMID: 31953512 PMC: 6969158. DOI: 10.1038/s41598-020-57480-2.

References

Lecharny A, Boudet N, Gy I, Aubourg S, Kreis M . Introns in, introns out in plant gene families: a genomic approach of the dynamics of gene structure. J Struct Funct Genomics. 2003; 3(1-4):111-6. View

Tang H, Bowers J, Wang X, Paterson A . Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc Natl Acad Sci U S A. 2009; 107(1):472-7. PMC: 2806719. DOI: 10.1073/pnas.0908007107. View

Auldridge M, McCarty D, Klee H . Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol. 2006; 9(3):315-21. DOI: 10.1016/j.pbi.2006.03.005. View

Rapp R, Wendel J . Epigenetics and plant evolution. New Phytol. 2005; 168(1):81-91. DOI: 10.1111/j.1469-8137.2005.01491.x. View

Gimenez M, Piston F, Atienza S . Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta. 2010; 233(1):163-73. DOI: 10.1007/s00425-010-1290-y. View

Atienza S, Ballesteros J, Martin A, Hornero-Mendez D . Genetic variability of carotenoid concentration and degree of esterification among tritordeum (xTritordeum Ascherson et Graebner) and durum wheat accessions. J Agric Food Chem. 2007; 55(10):4244-51. DOI: 10.1021/jf070342p. View

Aprile A, Mastrangelo A, De Leonardis A, Galiba G, Roncaglia E, Ferrari F . Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics. 2009; 10:279. PMC: 2713995. DOI: 10.1186/1471-2164-10-279. View

Kuchel H, Langridge P, Mosionek L, Williams K, Jefferies S . The genetic control of milling yield, dough rheology and baking quality of wheat. Theor Appl Genet. 2006; 112(8):1487-95. DOI: 10.1007/s00122-006-0252-z. View

Shen Q, Zhang P, Ho T . Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell. 1996; 8(7):1107-19. PMC: 161185. DOI: 10.1105/tpc.8.7.1107. View

10.

Howitt C, Cavanagh C, Bowerman A, Cazzonelli C, Rampling L, Mimica J . Alternative splicing, activation of cryptic exons and amino acid substitutions in carotenoid biosynthetic genes are associated with lutein accumulation in wheat endosperm. Funct Integr Genomics. 2009; 9(3):363-76. DOI: 10.1007/s10142-009-0121-3. View

11.

de Castro E, Sigrist C, Gattiker A, Bulliard V, Langendijk-Genevaux P, Gasteiger E . ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 2006; 34(Web Server issue):W362-5. PMC: 1538847. DOI: 10.1093/nar/gkl124. View

12.

Paine J, Shipton C, Chaggar S, Howells R, Kennedy M, Vernon G . Improving the nutritional value of Golden Rice through increased pro-vitamin A content. Nat Biotechnol. 2005; 23(4):482-7. DOI: 10.1038/nbt1082. View

13.

Flutre T, Duprat E, Feuillet C, Quesneville H . Considering transposable element diversification in de novo annotation approaches. PLoS One. 2011; 6(1):e16526. PMC: 3031573. DOI: 10.1371/journal.pone.0016526. View

14.

Zhang W, Dubcovsky J . Association between allelic variation at the Phytoene synthase 1 gene and yellow pigment content in the wheat grain. Theor Appl Genet. 2008; 116(5):635-45. DOI: 10.1007/s00122-007-0697-8. View

15.

Jaillon O, Aury J, Noel B, Policriti A, Clepet C, Casagrande A . The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007; 449(7161):463-7. DOI: 10.1038/nature06148. View

16.

Roy S, Gilbert W . The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet. 2006; 7(3):211-21. DOI: 10.1038/nrg1807. View

17.

Hunter S, Apweiler R, Attwood T, Bairoch A, Bateman A, Binns D . InterPro: the integrative protein signature database. Nucleic Acids Res. 2008; 37(Database issue):D211-5. PMC: 2686546. DOI: 10.1093/nar/gkn785. View

18.

Murat F, Xu J, Tannier E, Abrouk M, Guilhot N, Pont C . Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res. 2010; 20(11):1545-57. PMC: 2963818. DOI: 10.1101/gr.109744.110. View

19.

Quraishi U, Abrouk M, Bolot S, Pont C, Throude M, Guilhot N . Genomics in cereals: from genome-wide conserved orthologous set (COS) sequences to candidate genes for trait dissection. Funct Integr Genomics. 2009; 9(4):473-84. DOI: 10.1007/s10142-009-0129-8. View

20.

Welsch R, Wust F, Bar C, Al-Babili S, Beyer P . A third phytoene synthase is devoted to abiotic stress-induced abscisic acid formation in rice and defines functional diversification of phytoene synthase genes. Plant Physiol. 2008; 147(1):367-80. PMC: 2330301. DOI: 10.1104/pp.108.117028. View