Genomic and Biotechnology of the Fruits

Research Topics

The making of fruits comprises three main distinct stages known as fruit set, growth and maturation and in this regard, it offers a unique example of a series of developmental shifts tightly regulated by intricate signaling pathways that remain only partially understood. Building on the last period achievements, the GBF research project deals with the deciphering of the factors and mechanisms underlying the flower-to-fruit transition and the transition to ripening of flesh fruits using the tomato as a main model species. In the last period, GBF is also addressing the process of inflorescence meristem differentiation. GBF team addresses the link between hormone signaling and epigenetic regulation in controlling gene expression reprogramming during all these developmental processes. The group also investigates the genetic basis of the differentiation of fleshy tissues through the characterization of master regulators of fruit tissue texture, a major trait impacting quality and post-harvest behaviour. The elucidation of the processes of fruit setting and flower formation is fundamental to our understanding of reproductive organs biology and is anticipated to provide the basis for designing new breeding strategies to improve crop yield and fruit quality in the face of climate change. Likewise, fruit ripening is of prime importance as most sensory and nutritional quality traits take place during this ultimate phase of fruit development.

On the other hand, the GBF group continue to make a substantial contribution to the generation of generic resources and tools on the tomato model species through developing functional genomics platforms accessible to the scientific community. Building on the expertise gained on the tomato model, the group invested recently in the generation of genomic and transcriptomic resources on grape as a new fleshy fruit species. 

It is also worth mentioning that in support to its scientific programs, GBF is involved in major EU initiatives and is currently coordinating a COST European network dealing with the role of oxygen sensing in fleshy fruit ripening.

Fruit development consists of a series of developmental transitions, among which fruit ripening corresponds to the ultimate step, associated with seed maturation and dispersal. Tomato fruit is known to undergo climacteric ripening that is characterized by a sharp increase in respiration, the so-called “climacteric crisis”, and a rise in autocatalytic ethylene production. Ethylene is the main hormone controlling climacteric fruit ripening. While studies on ethylene are numerous, the mechanisms underlying the developmental transition leading to the initiation of the ripening process remains elusive, although it has been postulated that  an active hormone interplay  is involved in driving this process, as it is the case for fruit set (Chirinos et al 2022, Plant Phys.; An et al. 2020, Plant Science). In despite of the tremendous progress made in understanding the role of ethylene in controlling climacteric fruit ripening the putative link between the rise in respiration and the increase of ethylene production remains totally obscure. The elucidation made recently in the model plant Arabidopsis of the role of Ethylene Response Factors in oxygen sensing opened new prospects towards addressing the role of the increase in respiration during the climacteric ripening.

Ethylene receptors are encoded in the tomato by seven genes, named SlETR1 to SlETR7. Performing targeted proteomics analysis of ethylene tomato receptors, we recently showed that  ripening inhibition in the tomato may be associated with the increase of the ETR3 dominant mutated receptor (Chen et al. 2019, Frontiers Plant Sci.). Our data also revealed that ethylene sensing is critical for tomato pollen tube development, controlling at least cell wall metabolism and calcium signaling (Althiab-Almasaud et al., 2021a, Revue?).

The linear ethylene production and signaling cascade ultimately leads to the activation of members of the large Ethylene Response Factor (ERF) transcription factor family. Although it has been often  suggested that that ERFs are at the internode of different hormonal signaling pathways, data regarding the role of different hormones during the onset of ripening are still scarce. Using transcriptomics and hormone profiling approaches, we recently showed that  the transition to ripening is initiated in the tissues filling the locular cavities and that the transcriptomic reprogramming underlying this developmental shift requires a multi-hormonal control and a reformed auxin homeostasis, and most likely other hormones seems to be involved in this transitioning (Chirinos et al., 2022, Plant Phys.).

Softening and internal fruit structure are traits of prime importance for tomato sensory quality, postharvest behavior and overall commercial value. It is also a major criterion in determining whether the crop is better suited for fresh consumption or the processing industry. The dynamics of fleshy fruit tissue texture is complex, and softness has always been addressed as a ripening associated process. Notably, so far, all the strategies aiming at improving fruit texture and postharvest shelf-life consisted in attenuating the ripening process which inevitably leads to losses in sensory qualities resulting from incomplete ripening. It is noteworthy that “All-flesh” tomato cultivars are devoid of locular gel and exhibit enhanced firmness and improved postharvest storage. Our group aims to understand the process determining firmness and texture.  Although the deciphering of the components underlying the softening process has been mostly addressed by focusing on late stages of fruit development, our data are consistent with the notion that a large component of texture and firmness of ripe fruit is determined at early pre-ripening stages, concomitant with the initiation of inner tissues differentiation. Using reversed genetics, ChIPseq, transcritptomic and microscopy techniques we highlighted the role of MBP3, a class-D MADS-Box, in locular gel formation by controlling cell cycle and cell expansion genes, indicating that important components of fruit softening are determined at early pre-ripening stages. Our findings brings a paradigm shift of thinking and provides new opportunities for breeding strategies aiming to design tomato varieties, and possibly other fleshy fruits, with specific texture properties (Huang et al. 2021, Nature Com.). Such new varieties will be better suited for tomato processing and the extended shelf life of the fresh fruits will contribute to reducing wastage.

In flowering plants, differentiation of reproductive organs and successful flower fertilization are among the main determinants of crop yield, and in most crop species, yield relies primarily on the number of inflorescences and of flowers per inflorescence. Fruit set is naturally triggered by flower pollination and represents another important developmental process that impacts crop yield. Using the tomato as model species, we address the mechanisms of fruit set and inflorescence differentiation as two major steps determining fruit yield.

The transition from flower to fruit, the so-called fruit set, is an important determinant of crop yield and in the face of global warming and fast-growing world population, maintaining yield stability is becoming a major challenge. We investigate the epigenetic and transcriptomic reprogramming underlying pollination-dependent and auxin-induced flower-to-fruit transitions in the tomato (Solanum lycopersicum L.) using combined genome-wide transcriptomic profiling, global ChIP-sequencing and whole genomic DNA bisulfite sequencing (WGBS). Our data demonstrate reprogramming of genes involved in processes instrumental to fruit set correlated with their H3K9ac or H3K4me3 marking status but not with changes in cytosine methylation, indicating that histone post translational modifications rather than DNA methylation are associated with the remodeling of the epigenetic landscape underpinning the flower-to-fruit transition. Given the prominent role previously assigned to DNA methylation in reprogramming key genes of the transition to ripening, the outcome of the present study supports the idea that the two main developmental transitions in fleshy fruit and the underlying transcriptomic reprogramming are associated with different modes of epigenetic regulations (Hu et al. 2020, New Phytologist).

Understanding the mechanisms underlying differentiation of inflorescence and flower meristems is essential towards enlarging our knowledge of reproductive organ formation and to open new prospects for improving yield traits. Using CRISPR/Cas9 knock-out strategy, our recent study shows that SlDOF9 is a new modulator of floral differentiation in tomato. Our findings add a new actor to the complex mechanisms underlying reproductive organ differentiation in flowering plants and provide leads towards addressing the diversity of factors controlling the transition to reproductive organs (Hu et al 2022, Nature Plants).



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2: Wu CJ, Shan W, Liu XC, Zhu LS, Wei W, Yang YY, Guo YF, Bouzayen M, Chen JY, Lu WJ, Kuang JF. Phosphorylation of transcription factor bZIP21 by MAP kinase MPK6-3 enhances banana fruit ripening. Plant Physiol. 2022 Mar 4;188(3):1665-1685. doi: 10.1093/plphys/kiab539. PMID: 34792564; PMCID: PMC8896643.  

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5: Chirinos X, Ying S, Rodrigues MA, Maza E, Djari A, Hu G, Liu M, Purgatto E, Fournier S, Regad F, Bouzayen M, Pirrello J. Transition to ripening in tomato requires hormone-controlled genetic reprogramming initiated in gel tissue. Plant Physiol. 2023 Jan 2;191(1):610-625. doi: 10.1093/plphys/kiac464. PMID: 36200876; PMCID: PMC9806557.  

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Maury P, Latché A, Pech JC, Bouzayen M, Zouine M. SlARF4, an auxin response

factor involved in the control of sugar metabolism during tomato fruit

development. Plant Physiol. 2013 Mar;161(3):1362-74. doi: 10.1104/pp.113.213843.

Epub 2013 Jan 22. PMID: 23341361; PMCID: PMC3585602.


46: Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latché A, Pech

JC, Fernie AR, Bouzayen M. Regulatory features underlying pollination-dependent

and -independent tomato fruit set revealed by transcript and primary metabolite

profiling. Plant Cell. 2009 May;21(5):1428-52. doi: 10.1105/tpc.108.060830. Epub

2009 May 12. PMID: 19435935; PMCID: PMC2700536.


47: Bassa C, Mila I, Bouzayen M, Audran-Delalande C. Phenotypes associated with

down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family

members in tomato. Plant Cell Physiol. 2012 Sep;53(9):1583-95. doi:

10.1093/pcp/pcs101. Epub 2012 Jul 3. PMID: 22764281.


48: Maza E, Frasse P, Senin P, Bouzayen M, Zouine M. Comparison of normalization

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49: Egea I, Bian W, Barsan C, Jauneau A, Pech JC, Latché A, Li Z, Chervin C.

Chloroplast to chromoplast transition in tomato fruit: spectral confocal

microscopy analyses of carotenoids and chlorophylls in isolated plastids and

time-lapse recording on intact live tissue. Ann Bot. 2011 Aug;108(2):291-7. doi:

10.1093/aob/mcr140. PMID: 21788376; PMCID: PMC3143050.


50: Pirrello J, Jaimes-Miranda F, Sanchez-Ballesta MT, Tournier B, Khalil-Ahmad

Q, Regad F, Latché A, Pech JC, Bouzayen M. Sl-ERF2, a tomato ethylene response

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2006 Sep;47(9):1195-205. doi: 10.1093/pcp/pcj084. Epub 2006 Jul 20. PMID:



51: Manríquez D, El-Sharkawy I, Flores FB, El-Yahyaoui F, Regad F, Bouzayen M,

Latché A, Pech JC. Two highly divergent alcohol dehydrogenases of melon exhibit

fruit ripening-specific expression and distinct biochemical characteristics.

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52: Ambrosino L, Ruggieri V, Bostan H, Miralto M, Vitulo N, Zouine M, Barone A,

Bouzayen M, Frusciante L, Pezzotti M, Valle G, Chiusano ML. Multilevel

comparative bioinformatics to investigate evolutionary relationships and

specificities in gene annotations: an example for tomato and grapevine. BMC

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PMID: 30497367; PMCID: PMC6266932.


53: Barsan C, Zouine M, Maza E, Bian W, Egea I, Rossignol M, Bouyssie D,

Pichereaux C, Purgatto E, Bouzayen M, Latché A, Pech JC. Proteomic analysis of

chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled

with disrupted thylakoid biogenesis machinery and elevated energy-production

components. Plant Physiol. 2012 Oct;160(2):708-25. doi: 10.1104/pp.112.203679.

Epub 2012 Aug 20. PMID: 22908117; PMCID: PMC3461550.


54: Chervin C, Tira-Umphon A, Terrier N, Zouine M, Severac D, Roustan JP.

Stimulation of the grape berry expansion by ethylene and effects on related gene

transcripts, over the ripening phase. Physiol Plant. 2008 Nov;134(3):534-46.

doi: 10.1111/j.1399-3054.2008.01158.x. Epub 2008 Jul 31. PMID: 18785902.


55: El-Sharkawy I, Manríquez D, Flores FB, Regad F, Bouzayen M, Latché A, Pech

  1. Functional characterization of a melon alcohol acyl-transferase gene family

involved in the biosynthesis of ester volatiles. Identification of the crucial

role of a threonine residue for enzyme activity*. Plant Mol Biol. 2005

Sep;59(2):345-62. doi: 10.1007/s11103-005-8884-y. PMID: 16247561.


56: Lucchetta L, Manriquez D, El-Sharkawy I, Flores FB, Sanchez-Bel P, Zouine M,

Ginies C, Bouzayen M, Rombaldi C, Pech JC, Latché A. Biochemical and catalytic

properties of three recombinant alcohol acyltransferases of melon. sulfur-

containing ester formation, regulatory role of CoA-SH in activity, and sequence

elements conferring substrate preference. J Agric Food Chem. 2007 Jun

27;55(13):5213-20. doi: 10.1021/jf070210w. Epub 2007 Jun 2. PMID: 17542607.





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