A Third Phytoene Synthase Is Devoted to Abiotic Stress-Induced Abscisic Acid Formation in Rice and Defines Functional Diversification of Phytoene Synthase Genes  

Abstract

We here report on the characterization of a novel third phytoene synthase gene (PSY) in rice (Oryza sativa), OsPSY3, and on the differences among all three PSY genes with respect to the tissue-specific expression and regulation upon various environmental stimuli. The two already known PSYs are under phytochrome control and involved in carotenoid biosynthesis in photosynthetically active tissues and exhibit different expression patterns during chloroplast development. In contrast, OsPSY3 transcript levels are not affected by light and show almost no tissue-specific differences. Rather, OsPSY3 transcripts are up-regulated during increased abscisic acid (ABA) formation upon salt treatment and drought, especially in roots. The simultaneous induction of genes encoding 9-cis-epoxycarotenoid dioxygenases (NCEDs), involved in the initial steps of ABA biosynthesis, indicate that decreased xanthophyll levels are compensated by the induction of the third PSY gene. Furthermore, OsPSY3 and the OsNCEDs investigated were also induced by the application of ABA, indicating positive feedback regulation. The regulatory differences are mirrored by cis-acting elements in the corresponding promoter regions, with light-responsive elements for OsPSY1 and OsPSY2 and an ABA-response element as well as a coupling element for OsPSY3. The investigation of the gene structures and 5# untranslated regions revealed that OsPSY1 represents a descendant of an ancient PSY gene present in the common ancestor of monocots and dicots. Since the genomic structures of OsPSY2 and OsPSY3 are comparable, we conclude that they originated from the most recent common ancestor, OsPSY1.Carotenoids are lipophilic isoprenoids produced by all photosynthetic organisms as well as by some nonphotosynthetic bacteria and fungi. In animals, carotenoids come from the food chain and function as colorants and precursors for essential metabolites, such as retinal, retinol, and retinoic acid. In plants, carotenoids play their classical roles in light-harvesting complexes and photosynthetic reaction centers, where they absorb light and dissipate excess energy (for review, see Adams, 1992, 2000;Niyogi, 1999).The plant carotenoid biosynthetic pathway is localized in the plastid and has been molecularly elucidated in recent years (for review, see DellaPenna and Pogson, 2006). It diverges from C 3 carbon metabolism by the action of the enzyme deoxyxylulose phosphate synthase, followed by a series of enzymes of the socalled nonmevalonate pathway (for review, see Hunter, 2007), yielding isopentenyl diphosphate (IPP; C 5 ), the building block of all isoprenoids. IPP and its isomer dimethylallyl diphosphate (DMAPP) are then converted into carotenes through chain-elongating condensation reactions catalyzed by geranylgeranyl diphosphate synthase (GGPPS) and phytoene synthase (PSY; Fig. 1). The triene chromophore of phytoene (C 40 ), the first carotene formed, is then extended to form the colored undecaene in lycopene catalyzed by phytoene desaturase (PDS) and z-carotene desaturase (ZD...

Carotenoids in nature: insights from plants and beyond

“…In addition to high light, PSY can be transcriptionally responsive to ABA, salt, drought, temperature, photoperiod, development cues and post-transcriptional feedback regulation . Carotenoid pathway flux can be controlled by multiple PSYs, as is the case for tomato, rice and maize, whereas only a single allele exists in Arabidopsis (Welsch et al , 2008Giorio et al 2008;Li et al 2008a). Multiple homologues of PSY are likely to be somewhat redundant; however, individual PSY alleles are expressed in a tissue-specific manner and only some alleles show a unique response to abiotic stress-induced ABA signalling of PSY gene expression (Li et al 2008b;Welsch et al 2008;Qin et al 2011).…”

“…Carotenoid pathway flux can be controlled by multiple PSYs, as is the case for tomato, rice and maize, whereas only a single allele exists in Arabidopsis (Welsch et al , 2008Giorio et al 2008;Li et al 2008a). Multiple homologues of PSY are likely to be somewhat redundant; however, individual PSY alleles are expressed in a tissue-specific manner and only some alleles show a unique response to abiotic stress-induced ABA signalling of PSY gene expression (Li et al 2008b;Welsch et al 2008;Qin et al 2011). Alternative splicing as well as allelic variation are mechanisms by which to titrate PSY enzyme activity and are likely to underlie a major QTL determinant of flour colour pathway in chloroplasts provides C 20 isoprenoid substrates for carotenoid biosynthesis.…”

Timing and Biosynthetic Potential for Carotenoid Accumulation in Genetically Diverse Germplasm of Maize

“…The DXS phylogenetic tree (Fig. 3A) showed that the DXS triplication occurred prior to evolution of the grasses, suggesting that grass orthologs may have similar subfunctionalized roles, as shown for the PSY gene family (Li et al, 2008a(Li et al, , 2009Welsch et al, 2008). Therefore DXS3 orthologs in other grass species would be an attractive target for initiating investigations of ratecontrolling steps for endosperm isoprenoid-derived metabolites.…”

The Maize Phytoene Synthase Gene Family: Overlapping Roles for Carotenogenesis in Endosperm, Photomorphogenesis, and Thermal Stress Tolerance

“…Maize PSY1 and PSY3 did not respond to light of any spectral type. It was previously demonstrated that PSY3 was associated with carotenogenesis leading to drought and salt-induced ABA biosynthesis in roots (Li et al, 2008); recent work on rice PSY3 showed the rice homolog to have a similar role in rice roots (Welsch et al, 2008). Unlike maize, rice PSY1 and PSY2 are both photoregulated, although blue light was not tested (Welsch et al, 2008), and rice PSY1 is not expressed in endosperm (Gallagher et al, 2004).…”

“…It was previously demonstrated that PSY3 was associated with carotenogenesis leading to drought and salt-induced ABA biosynthesis in roots (Li et al, 2008); recent work on rice PSY3 showed the rice homolog to have a similar role in rice roots (Welsch et al, 2008). Unlike maize, rice PSY1 and PSY2 are both photoregulated, although blue light was not tested (Welsch et al, 2008), and rice PSY1 is not expressed in endosperm (Gallagher et al, 2004). Therefore, the ancestral Poaceae PSY was a photoregulated gene; the duplications analyzed in Y1 maize represent losses in the photoregulatory mechanisms and evolution of other features, including the gain-of-function endosperm-specific expression seen for PSY1 in Y1 maize, but absent in its evolutionary ancestor teosinte and other subfamilies of the grasses, including species such as rice.…”