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Expression profiling of cell cycle genes reveals key facilitators of cell production during carpel development, fruit set, and fruit growth in apple (Malusxdomestica Borkh.).

ABSTRACT: Cell production is an essential facilitator of fruit growth and development. Cell production during carpel/floral-tube growth, fruit set, and fruit growth, and its regulation by cell cycle genes were investigated in apple (Malus×domestica Borkh.). Cell production was inhibited during late carpel/floral-tube development, resulting in growth arrest before bloom. Fruit set re-activated cell production between 8 d and 11 d after full bloom (DAFB) and triggered fruit growth. The early phase of fruit growth involved rapid cell production followed by exit from cell proliferation at ?24 DAFB. Seventy-one cell cycle genes were identified, and expression of 59 genes was investigated using quantitative RT-PCR. Changes in expression of 19 genes were consistently associated with transitions in cell production during carpel/floral-tube growth, fruit set, and fruit growth. Fourteen genes, including B-type cyclin-dependent kinases (CDKs) and A2-, B1-, and B2-type cyclins, were positively associated with cell production, suggesting that availability of G2/M phase regulators of the cell cycle is limiting for cell proliferation. Enhanced expression of five genes including that of the putative CDK inhibitors, MdKRP4 and MdKRP5, was associated with reduced cell production. Exit from cell proliferation at G0/G1 during fruit growth was facilitated by multiple mechanisms including down-regulation of putative regulators of G1/S and G2/M phase progression and up-regulation of KRP genes. Interestingly, two CDKA genes and several CDK-activating factors were up-regulated during this period, suggesting functions for these genes in mediating exit from cell proliferation at G0/G1. Together, the data indicate that cell cycle genes are important facilitators of cell production during apple fruit development.

SUBMITTER: Malladi A

PROVIDER: S-EPMC2993910 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

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Expression profiling of cell cycle genes reveals key facilitators of cell production during carpel development, fruit set, and fruit growth in apple (Malusxdomestica Borkh.).

Malladi Anish A Johnson Lisa Klima LK

Journal of experimental botany 20100822 1

Cell production is an essential facilitator of fruit growth and development. Cell production during carpel/floral-tube growth, fruit set, and fruit growth, and its regulation by cell cycle genes were investigated in apple (Malus×domestica Borkh.). Cell production was inhibited during late carpel/floral-tube development, resulting in growth arrest before bloom. Fruit set re-activated cell production between 8 d and 11 d after full bloom (DAFB) and triggered fruit growth. The early phase of fruit ...[more]

PMID: 20732881

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Project description:KEY MESSAGE:Comparative ultrastructural developmental time-course analysis has identified discrete stages at which the fruit plastids undergo structural and consequently functional transitions to facilitate subsequent development-guided understanding of the complex plastid biology. Plastids are the defining organelle for a plant cell and are critical for myriad metabolic functions. The role of leaf plastid, chloroplast, is extensively documented; however, fruit plastids-chromoplasts-are poorly understood, especially in the context of the diverse metabolic processes operating in these diverse plant organs. Recently, in a comparative study of the predicted plastid-targeted proteomes across seven plant species, we reported that each plant species is predicted to harbor a unique set of plastid-targeted proteins. However, the temporal and developmental context of these processes remains unknown. In this study, an ultrastructural analysis approach was used to characterize fruit plastids in the epidermal and collenchymal cell layers at 11 developmental timepoints in three genotypes of apple (Malus × domestica Borkh.): chlorophyll-predominant 'Granny Smith', carotenoid-predominant 'Golden Delicious', and anthocyanin-predominant 'Top Red Delicious'. Plastids transitioned from a proplastid-like plastid to a chromoplast-like plastid in epidermis cells, while in the collenchyma cells, they transitioned from a chloroplast-like plastid to a chloro-chromo-amyloplast plastid. Plastids in the collenchyma cells of the three genotypes demonstrated a diverse array of structures and features. This study enabled the identification of discrete developmental stages during which specific functions are most likely being performed by the plastids as indicated by accumulation of plastoglobuli, starch granules, and other sub-organeller structures. Information regarding the metabolically active developmental stages is expected to facilitate biologically relevant omics studies to unravel the complex biochemistry of plastids in perennial non-model systems.

Project description:BackgroundFruit growth in apple (Malus × domestica Borkh.) is mediated by cell production and expansion. Genes involved in regulating these processes and thereby fruit growth, are not well characterized. We hypothesized that the apple homolog(s) of AINTEGUMENTA (ANT), an APETALA2-repeat containing transcription factor, regulates cell production during fruit growth in apple.ResultsTwo ANT genes, MdANT1 and MdANT2, were isolated from apple and their expression was studied during multiple stages of fruit development. MdANT1 and MdANT2 expression was high during early fruit growth coincident with the period of cell production, rapidly declined during exit from cell production, and remained low during the rest of fruit development. The effects of increase in carbohydrate availability during fruit growth were characterized. Increase in carbohydrate availability enhanced fruit growth largely through an increase in cell production. Expression of MdANT1 and MdANT2 increased sharply by up to around 5-fold in response to an increase in carbohydrate availability. Expression of the ANT genes was compared across two apple genotypes, 'Gala' and 'Golden Delicious Smoothee' (GS), which differ in the extent of fruit growth, largely due to differences in cell production. In comparison to 'Gala', the larger fruit-size genotype, GS, displayed higher levels and a longer duration of MdANT1 and MdANT2 expression. Expression of the ANTs and cell cycle genes in the fruit core and cortex tissues isolated using laser capture microdissection was studied. During early fruit growth, expression of the MdANTs was higher within the cortex, the tissue that constitutes the majority of the fruit. Additionally, MdANT1 and MdANT2 expression was positively correlated with that of A- and B-type CYCLINS, B-type CYCLIN-DEPENDENT-KINASES (CDKBs) and MdDEL1.ConclusionsMultiple lines of evidence from this study suggest that MdANT1 and MdANT2 regulate cell production during fruit growth in apple. ANTs may coordinate the expression of cell proliferation genes and thereby affect the competence of cells for cell production during fruit growth. Together, data from this study implicate MdANT1 and MdANT2 in the regulation of fruit growth in apple.

Dataset Information

Expression profiling of cell cycle genes reveals key facilitators of cell production during carpel development, fruit set, and fruit growth in apple (Malusxdomestica Borkh.).

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Expression profiling of cell cycle genes reveals key facilitators of cell production during carpel development, fruit set, and fruit growth in apple (Malusxdomestica Borkh.).

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