Transcriptome Profiling Reveals the Regulatory Mechanism Underlying Pollination Dependent and Parthenocarpic Fruit Set Mainly Mediated by Auxin and Gibberellin

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2015 Apr 25

PMID 25909657

Citations 34

Authors

Ning Tang

Wei Deng

Guojian Hu

Nan Hu

Zhengguo Li

Affiliations

Soon will be listed here.

Abstract

Background: Fruit set is a key process for crop production in tomato which occurs after successful pollination and fertilization naturally. However, parthenocarpic fruit development can be uncoupled from fertilization triggered by exogenous auxin or gibberellins (GAs). Global transcriptome knowledge during fruit initiation would help to characterize the molecular mechanisms by which these two hormones regulate pollination-dependent and -independent fruit set.

Principal Findings: In this work, digital gene expression tag profiling (DGE) technology was applied to compare the transcriptomes from pollinated and 2, 4-D/GA3-treated ovaries. Activation of carbohydrate metabolism, cell division and expansion as well as the down-regulation of MADS-box is a comprehensive regulatory pathway during pollination-dependent and parthenocarpic fruit set. The signaling cascades of auxin and GA are significantly modulated. The feedback regulations of Aux/IAAs and DELLA genes which functioned to fine-tune auxin and GA response respectively play fundamental roles in triggering fruit initiation. In addition, auxin regulates GA synthesis via up-regulation of GA20ox1 and down-regulation of KNOX. Accordingly, the effect of auxin on fruit set is mediated by GA via ARF2 and IAA9 down-regulation, suggesting that both pollination-dependent and parthenocarpic fruit set depend on the crosstalk between auxin and GA.

Significance: This study characterizes the transcriptomic features of ovary development and more importantly unravels the integral roles of auxin and GA on pollination-dependent and parthenocarpic fruit set.

Citing Articles

Editorial: Transcriptomics of fruit growth, development and ripening.

Ochoa-Alejo N, Gomez-Jimenez M, Martinez O Front Plant Sci. 2024; 15:1399376.

PMID: 38645390 PMC: 11026863. DOI: 10.3389/fpls.2024.1399376.

Preliminary Study on the Formation Mechanism of Malformed Sweet Cherry ( L.) Fruits in Southern China Using Transcriptome and Metabolome Data.

Zhang W, Xu Y, Jing L, Jiang B, Wang Q, Wang Y Int J Mol Sci. 2024; 25(1).

PMID: 38203324 PMC: 10779264. DOI: 10.3390/ijms25010153.

Parthenocarpy in : Advances for Economic and Environmental Sustainability.

Tian S, Zhang Z, Qin G, Xu Y Plants (Basel). 2023; 12(19).

PMID: 37836203 PMC: 10574560. DOI: 10.3390/plants12193462.

Four class A AUXIN RESPONSE FACTORs promote tomato fruit growth despite suppressing fruit set.

Hu J, Li X, Sun T Nat Plants. 2023; 9(5):706-719.

PMID: 37037878 PMC: 10276352. DOI: 10.1038/s41477-023-01396-y.

Modulating auxin response stabilizes tomato fruit set.

Israeli A, Schubert R, Man N, Teboul N, Serrani Yarce J, Rosowski E Plant Physiol. 2023; 192(3):2336-2355.

PMID: 37032117 PMC: 10315294. DOI: 10.1093/plphys/kiad205.

References

Vriezen W, Feron R, Maretto F, Keijman J, Mariani C . Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytol. 2007; 177(1):60-76. DOI: 10.1111/j.1469-8137.2007.02254.x. View

Serrani J, Ruiz-Rivero O, Fos M, Garcia-Martinez J . Auxin-induced fruit-set in tomato is mediated in part by gibberellins. Plant J. 2008; 56(6):922-34. DOI: 10.1111/j.1365-313X.2008.03654.x. View

Morrissy A, Morin R, Delaney A, Zeng T, McDonald H, Jones S . Next-generation tag sequencing for cancer gene expression profiling. Genome Res. 2009; 19(10):1825-35. PMC: 2765282. DOI: 10.1101/gr.094482.109. View

t Hoen P, Ariyurek Y, Thygesen H, Vreugdenhil E, Vossen R, de Menezes R . Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res. 2008; 36(21):e141. PMC: 2588528. DOI: 10.1093/nar/gkn705. View

Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M . Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science. 2003; 299(5614):1896-8. DOI: 10.1126/science.1081077. View

Jin Y, Ni D, Ruan Y . Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell. 2009; 21(7):2072-89. PMC: 2729613. DOI: 10.1105/tpc.108.063719. View

Zhu H, Hu F, Wang R, Zhou X, Sze S, Liou L . Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell. 2011; 145(2):242-56. PMC: 4124879. DOI: 10.1016/j.cell.2011.03.024. View

Mounet F, Moing A, Kowalczyk M, Rohrmann J, Petit J, Garcia V . Down-regulation of a single auxin efflux transport protein in tomato induces precocious fruit development. J Exp Bot. 2012; 63(13):4901-17. PMC: 3427993. DOI: 10.1093/jxb/ers167. View

Pnueli L, Hareven D, Rounsley S, Yanofsky M, Lifschitz E . Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell. 1994; 6(2):163-73. PMC: 160424. DOI: 10.1105/tpc.6.2.163. View

10.

Olimpieri I, Siligato F, Caccia R, Mariotti L, Ceccarelli N, Soressi G . Tomato fruit set driven by pollination or by the parthenocarpic fruit allele are mediated by transcriptionally regulated gibberellin biosynthesis. Planta. 2007; 226(4):877-88. DOI: 10.1007/s00425-007-0533-z. View

11.

Serrani J, Sanjuan R, Ruiz-Rivero O, Fos M, Garcia-Martinez J . Gibberellin regulation of fruit set and growth in tomato. Plant Physiol. 2007; 145(1):246-57. PMC: 1976567. DOI: 10.1104/pp.107.098335. View

12.

Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F . The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell. 2005; 17(10):2676-92. PMC: 1242265. DOI: 10.1105/tpc.105.033415. View

13.

Mazzucato A, Olimpieri I, Siligato F, Picarella M, Soressi G . Characterization of genes controlling stamen identity and development in a parthenocarpic tomato mutant indicates a role for the DEFICIENS ortholog in the control of fruit set. Physiol Plant. 2008; 132(4):526-37. DOI: 10.1111/j.1399-3054.2007.01035.x. View

14.

Kolotilin I, Koltai H, Tadmor Y, Bar-Or C, Reuveni M, Meir A . Transcriptional profiling of high pigment-2dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiol. 2007; 145(2):389-401. PMC: 2048735. DOI: 10.1104/pp.107.102962. View

15.

Marti C, Orzaez D, Ellul P, Moreno V, Carbonell J, Granell A . Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J. 2007; 52(5):865-76. DOI: 10.1111/j.1365-313X.2007.03282.x. View

16.

Gillaspy G, Ben-David H, Gruissem W . Fruits: A Developmental Perspective. Plant Cell. 1993; 5(10):1439-1451. PMC: 160374. DOI: 10.1105/tpc.5.10.1439. View

17.

Carbonell-Bejerano P, Urbez C, Granell A, Carbonell J, Perez-Amador M . Ethylene is involved in pistil fate by modulating the onset of ovule senescence and the GA-mediated fruit set in Arabidopsis. BMC Plant Biol. 2011; 11:84. PMC: 3124430. DOI: 10.1186/1471-2229-11-84. View

18.

Ding J, Chen B, Xia X, Mao W, Shi K, Zhou Y . Cytokinin-induced parthenocarpic fruit development in tomato is partly dependent on enhanced gibberellin and auxin biosynthesis. PLoS One. 2013; 8(7):e70080. PMC: 3726760. DOI: 10.1371/journal.pone.0070080. View

19.

Richter R, Behringer C, Zourelidou M, Schwechheimer C . Convergence of auxin and gibberellin signaling on the regulation of the GATA transcription factors GNC and GNL in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2013; 110(32):13192-7. PMC: 3740866. DOI: 10.1073/pnas.1304250110. View

20.

Saldanha A . Java Treeview--extensible visualization of microarray data. Bioinformatics. 2004; 20(17):3246-8. DOI: 10.1093/bioinformatics/bth349. View