Neftali Ochoa-Alejo
Maria Carmen Gómez-Jiménez
Octavio Martínez- 1Departamento de Ingeniería Genética, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Irapuato, Irapuato, Guanajuato, Mexico
- 2Laboratory of Plant Physiology, Universidad de Extremadura, Badajoz, Spain
- 3Unidad de Genómica Avanzada, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Guanajuato, Mexico
Editorial on the Research Topic
Transcriptomics of fruit growth, development and ripening
Introduction
Fruits are organs that hold seeds in plant species. From a botanical point of view, fruit is defined as a mature ovary (Roth, 1977), or as a structure developing from the gynoecium of one flower as the result of pollination or parthenocarpy (Bobrov and Romanov, 2019), or, additionally, as the flower in the state of seed germination (Knoll, 1939). An enormous variety of fruits with different forms, sizes, textures, colors, flavors, and aromas exists in nature (Klee, 2010; Rodríguez et al., 2012; Stournaras et al., 2012; Wu et al., 2018; Kapoor et al., 2022). Fruits are classified as fleshy or dry. Fleshy fruits are distributed in nature primarily by animals, whereas dry fruits may be dispersed by animals, wind, or water (Carey et al., 2019). Dry fruits are classified as dehiscent when they release seeds into environment (the seeds are discarded before or after consuming), or indehiscent those that release seeds in protected fruit wall propagules. Fleshy fruits are classified as climacteric (bananas, tomatoes, apricot, pears, mangoes, apricots, peaches, apples, papayas, guava, nectarines, blueberry, plum, passion fruit, cantaloupe, and avocados) or non-climacteric (grapefruit and lemon, berries such as raspberry, strawberry, cherry, grapes, pineapple, melon, watermelon, and pomegranate). In climacteric fruits, a burst of ethylene biosynthesis and an increase in respiration is observed at the onset of ripening. On the other hand, non-climacteric fruits lack the autocatalytic ethylene burst. Fruits are plant organs of nutritional value for animals and humans since they are sources of food, fiber, vitamins, minerals, carbohydrates, organic acids, amino acids, proteins, polyphenols (flavonoids and stilbenes), sterols, fatty acids, lipids, and pigments with antioxidant properties, among others (McKee and Latner, 2000; Zamora et al., 2001; Avila-Sosa et al., 2019; Wu et al., 2019; Golovinskaia and Wang, 2021; Alvi et al., 2022; Kasampalis et al., 2022; Yun et al., 2022; Bures et al., 2023; Cavalcante de Oliveira et al., 2023). Fruits are formed from single ovaries and may or may not involve inclusion of accessory floral tissues like the floral receptacle. After pollination, flowers undergo complex processes involving cell division, cell enlargement, and cell differentiation mediated by the expression of hundreds or even thousands of genes under a fine, harmonic, and sequentially regulated program to promote growth, development, ripening and, finally, senescence (Gillaspy et al., 1993; Karlova et al., 2014). Fruit initiation, growth, development, ripening, and senescence are influenced by genetic, epigenetic, hormonal, and environmental factors (Seymour et al., 2008, 2013; Chen et al., 2022). A powerful approach to study those genes expressed during the growth, development, ripening, and senescence is transcriptomics through RNA-Seq analysis (Wang et al., 2009; Tarazona et al., 2011; Trapnell et al., 2013; Li D, et al., 2022). The set of all RNA molecules transcribed in an organ or tissue at a particular point of time under a given set of environmental conditions constitute the transcriptome (Velculescu et al., 1997; Martínez-López et al., 2014). Arabidopsis thaliana and tomato (Solanum lycopersicum) have been used as model plants to investigate dry and fleshy fruit biology, respectively (Seymour et al., 2013; Gómez et al., 2014). This Research Topic focuses on transcriptomic research in different plant species revealing changes in gene expression and key regulatory gene networks involved in fruit growth, development, ripening, and senescence.
Fruit transcriptomics
Transcriptional changes in fleshy fruits during growth, development, and ripening were previously reviewed (Karlova et al., 2014); transcriptomic analysis of the dry fruit (silique) of the model plant Arabidopsis thaliana was published by Mizzotti et al. (2018). In general, fruit formation, development, ripening, and senescence involve metabolic changes regulated by hormones and environmental factors; these changes include variations in metabolites, color, flavor, and aroma, and the softening process in the case of fleshy fruits. All these changes are usually regulated at the transcriptional level by diverse transcription factors (TFs). Transcriptional studies on fruit growth, development, ripening, and senescence have been published by different authors for several tropical plant species, including mango (Mangifera indica L.) (Pandit et al., 2010), pineapple (Ananas comosus) (Koia et al., 2012), melon (Cucumis melo L.) (Saladié et al., 2015), watermelon [Citrullus lanatus (Thunb.) Matsun. & Nakai)] (Zhu et al., 2017), litchi (Litchi chinensis Sonn.) (Liu et al., 2017), citrus (Citrus sinensis) (Feng et al., 2019), and goji berry (Lycium barbarum) (Zhao et al., 2020), or on temperate species such as almond (Prunus dulcis) (Guo et al., 2021), apple (Malus domestica) (Xu et al., 2020; Li M, et al., 2022), peach (Prunus persica) (Li M, et al., 2022), pear (Pyrus spp.) (Xie et al., 2013; Zhang et al., 2016), blueberry (Vaccinia spp.) (Gao et al., 2021; Yang L, et al., 2021), grape berry (Vitis vinifera) (Minio et al., 2019), and raspberry (Rubus idaeus) and strawberry (Fragaria vesca) (Zhou et al., 2023), have been reported. Transcriptomics of fruits used as vegetables, such as cucumber (Cucumber sativus), and chili pepper (Capsicum spp.), have been also published (Ando et al., 2012; Martínez et al., 2021, respectively). As an example of transcriptomic analysis, Galla et al. (2009) described a computational annotation of differentially expressed genes in fruits of olive (Olea europea L. cv. Leccino), a non-climacteric species, at three developmental stages (initial fruit set, completed pit hardening, and veraison) using subtractive hybridization libraries; 1,132 clones were sequenced, 60% of which presented similarity with known proteins, and were annotated by Gene Ontology (GO). Bioinformatic analysis revealed a significantly different distribution of the annotated GO category. The olive fruit-specific transcriptome dataset was used to query all known KEGG (Kyoto Encyclopedia of Genes and Genomes) metabolic pathways for characterizing and positioning retrieved EST (Expressed Sequence Tags) records, finding a predominance of KEGS maps associated to carbohydrate (enzymes involved in starch and sucrose metabolism, glycolysis and gluconeogenesis), fatty acid (fatty acid biosynthesis and lipid degradation), and secondary metabolism (phenylpropanoids, terpenoids, flavonoids, alkaloids, and caffeine biosynthesis, and limonene and pinene degradation). Moreover, genes involved in amino acid biosynthesis and metabolism were also differentially expressed. Genes related to hormone biosynthesis and action were also found to be differentially expressed. Auxin responsive transcription factor genes, such as ARF1 and ARF7, were up- and down-regulated, respectively. Biosynthesis of abscisic acid (ABA) was stimulated as well as the expression of the ABA-biosynthesis related enzyme genes ABA2 (ABA DEFICIENT 2), and AAO3 (ABSCISIC ALDEHYDE OXIDASE). Genes related to the biosynthesis and action of indoleacetic acid (IAA), ABA, gibberellic acid (GA), ethylene, cytokinins, jasmonate, and salicylic acid were differently regulated according to the type of hormone. Genes encoding transcription factors were mainly down-regulated throughout fruit development, while some others were related to protein modification and degradation. In a further study (Parra et al., 2013), a comparative transcriptional profiling analysis of pericarp and the abscission zone (AZ) tissues in olive ripe-fruit from cv. Picual was conducted, and it was found that 4,391 genes were differentially expressed (DEG); in general, AZ tissue exhibited higher response to external stimuli than did ripe fruit, with higher expression of auxin-signaling genes, lignin catabolic and biosynthetic pathway, and of biosynthetic pathways of aromatic amino acid, isoprenoids, protein amino acid dephosphorylation, photosynthesis, and amino acid transport. Ripe fruit showed an enrichment in transcripts involved in ATP synthesis coupled proton transport, glycolysis, and cell-wall organization. Additionally, approximately 150 transcripts encoding putative TFs of diverse families were identified (37 fruit TFs and 113 AZ TFs); the most abundant TFs in ripe fruit were MADS-box proteins (TAGL2, AGL9, AG1), homeobox domain proteins, zinc finger proteins (ZF), basic helix-loop-helix proteins (bHLH), and basic leucine zipper proteins (bZIP). Among the 37 TF genes, 25 were exclusively expressed in fruit [6 ZF, 5 homeobox proteins, 5 bHLH domain class, 3 bZIP, 1 MADS-box (AG1), 1 MYB (MYBA22), 1 NAC, 1 Aux/IAA (IAA1), 1 CAMTA, and 1 C2H21. In the AZ tissue ZF, bHLH, and bZIP genes were highly expressed, but at different proportions, and one member of the E2F family and 9 WRKY TFs genes were exclusively expressed.
In some cases, transcriptional studies have been focused on just early or late stages of fruit development and ripening (Ando et al., 2012; Gómez et al., 2014; Liu et al., 2017), or on a specific tissue (Parra et al., 2013; Tafolla-Arellano et al., 2017; Luo et al., 2018; Zhang et al., 2021; Zhou et al., 2022), or even on cell transcriptomics (Martin et al., 2016; Shinozaki et al., 2018). Moreover, transcriptomics of hormones-related gene expression (Zhu et al., 2011; Huang et al., 2014; Van de Poel et al., 2014; Tang et al., 2015; Briegas et al., 2020; Kou et al., 2021; Qiao et al., 2021; Camarero et al., 2023), or the effects of environmental/stress factors on fruit gene expression (Li et al., 2019; Cramer et al., 2020; Waite et al., 2023), biosynthesis/metabolism genes expressed during fruit development (Yu et al., 2021; Zhang et al., 2021; Diao et al., 2023), transcriptomic changes due to the evolution/domestication processes (Martínez et al., 2021; Borredá et al., 2022; Gramzou et al., 2022), expression of transcription factors genes and gene networks (Ye et al., 2015; Villa-Rivera et al., 2022), transcriptomics of fruit quality (Yang H, et al., 2021; Lei et al., 2022), fruit shape (Tsaballa et al., 2011; Shi et al., 2023) and size-related genes (Huang et al., 2023; Liu et al., 2023), or postharvest transcriptomic changes (Wang et al., 2018; Romero et al., 2022), have been documented as an approach to reveal the mechanisms and factors involved in the growth, development, ripening, and senescence of fruits.
Articles and insights
This Research Topic is composed of nine articles, and among them, two deal with different aspects of fruit transcriptomics, including growth, development, and ripening (Gaete-Eastman et al.; Rajewski et al.), and in one case the transcriptomic analysis was combined with metabolomics to study fruit flavor (Lu et al.). Basically, Rajewski et al. looked for differentially expressed genes in pericarp tissues of dry fruits from Nicotiana obtusifolia and Solanum pimpinellifolium, two wild species, and of the fleshy fruits from Solanum lycopersicum and Cucumis melo, two climacteric species, and, interestingly, they found core genes (121) during fruit development and ripening when Arabidopsis thaliana fruits (dry) were also included in the analysis; on the other hand, in the comparative gene expression profiles between the wild tomato (S. pimpinellifolium) and the domesticated species (S. lycopersicum), 1,472 genes showed divergent expression patterns and there were Gene Ontology enrichments for plant-type cell wall organization and lipid biosynthetic processes. Furthermore, expression analysis of ethylene, pigment, and flavor biosynthesis-related genes exhibited statistically significant differences between cultivated and wild tomato. Additionally, fruit size-, firmness-, and lignification-related transcription factors differed in expression between wild and domesticated tomato. This study revealed insights on the effects of domestication on gene expression profiles and on the evolutionary process in dry and fleshy fruits. In another article, Gaete-Eastman et al. reported an RNA-Seq transcriptomic analysis across different developmental stages and ripening of the non-climacteric fruits of Fragaria chiloensis, a Chilean strawberry species, and the main findings refer to the differential expression of ABA biosynthesis-related genes involved in softening, color, and aroma production, which are regulated by transcription factors such as FcMYB1. In an integrated metabolomic and transcriptomic study of jujube (Ziziphus jujuba) fruits during development and maturation, Lu et al., described differentially expressed transcription factor genes highly correlated with sugars and organic acids accumulation, important compounds involved in the fruit flavor.
Two articles were focused on the expression analysis of specific gene families during fruit development and ripening (Cai et al.; Dhar et al.). A genome-wide analysis of histone acetyltransferase (HAT) and histone deacetylase (HDAC) gene families and their expression in chili pepper (Capsicum annuum L.) fruits during development and ripening revealed a total of 30 HAT and 15 HDAC, which were differentially expressed and may be involved in the regulation of fruit development- and ripening-related phytohormone metabolism and signaling through changes in chromatin acetylation/deacetylation activities (Cai et al.). In the other case, Dhar et al. reported a genome and transcriptome-wide analysis of carbamoyltransferase genes (play roles by regulating the urea cycle, de novo pyrimidine biosynthesis, and arginine biosynthesis in prokaryotes and eucaryotes) in major fleshy fruits (30) from an evolutionary point of view, and they found 393 carbamoyltransferase genes conserved in the plant kingdom, indicating a fundamental biological relevance.
Additionally, the overexpression of the carotenoid biosynthesis-related structural gene PSY1 as an approach to increase the carotenoid content in the skin and flesh of apple (Malus domestica) fruits was investigated, and an increase in carotenoid content (β-carotene being the most accumulated) was observed (Ampomah-Dwamena et al.).
A postharvest molecular study on the climacteric apple (Malus domestica cv. Golden Delicious) fruit quality after wax coating treatment was reported here, and the main findings were the inhibition of the expression of ethylene biosynthesis, chlorophyl degradation, and carotenoid biosynthesis-related genes (Si et al.). In one article, key genes associated with seed germination dormancy as affected by cold stratification in Fritillaria taipaiensis P.Y.Li (a traditional Chinese medicinal plant) were analyzed and they found that stratification at 4 °C induced an up-regulation of genes involved in gibberellic acid and auxin biosynthesis (Yang et al.). Finally, a comparative transcriptomic analysis between plants bearing prickles and non-prickled plants revealed the possible developmental mechanism of prickle formation in the important forest species Zanthoxylum bungeanum (Su et al.).
In conclusion, this Research Topic included not only interesting articles on transcriptomics covering different aspects of growth, development, and ripening of fruits from different plant species, but involving even transcriptomic changes occurring during postharvest conditions and germination of seeds, which certainly will be of motivation for those researchers working on this important biological process.
Author contributions
NO-A: Conceptualization, Funding acquisition, Investigation, Visualization, Writing – original draft, Writing – review & editing. MG-J: Writing – review & editing. OM: Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. The author(s) thank Consejo Nacional de Humanidades, Ciencias y Tecnologías (Conahcyt, Mexico) for the financial support through the project FC1570.
Acknowledgments
We would like to express our gratitude to Frontiers in Plant Science for giving us the opportunity to be Guest Editors for the Research Topic “Transcriptomics of fruit growth, development and ripening”. Our plenty gratitude also goes to all authors, contributors and experts who have played a significant role in making this Research Topic a valuable and engaging resource.
Conflict of interest
The authors declare that this Editorial was elaborated in the absence of any commercial or financial relationships that could be constructed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Alvi, T., Khan, M. K. I., Maan, A. I., Razzaq, Z. U. (2022). Date fruit as a promising source of functional carbohydrates and bioactive compounds: A review on its nutraceutical potential. J. Food Biochem. 46, e14325. doi: 10.1111/jfbc.14325
Ando, K., Carr, K. M., Grumet, R. (2012). Transcriptome analyses of early cucumber fruit growth identifies distinct gene modules associated with phases of development. BMC Genomics 13, 518. doi: 10.1186/1471-2164-13-518
Avila-Sosa, R., Montero-Rodríguez, A. F., Aguilar-Alonso, P., Vera-López, O., Lazcano-Hernández, M., Morales-Medina, J. C., et al. (2019). Antioxidant properties of Amazonian fruits: A mini review of in vivo and in vitro studies. Oxid. Med. Cell. Longev. 2019, 8204129. doi: 10.1155/2019/8204129
Bobrov, A. V. F. C., Romanov, M. S. (2019). Morphogenesis of fruits and types of fruit of angiosperms. Bot. Lett. 166, 366–399. doi: 10.1080/23818107.2019.1663448
Borredá, C., Perez-Roma, E., Talon, M., Terol, J. (2022). Comparative transcriptomics of wild and commercial Citrus during early ripening reveals how domestication shaped fruit gene expression. BMC Plant Biol. 22, 123. doi: 10.1186/s12870-022-03509-9
Briegas, B., Corbacho, J., Parra-Lobato, M. C., Paredes, M. A., Labrador, J., Gallardo, M., et al. (2020). Transcriptome and hormone analyses revealed insights into hormonal and vesicle trafficking regulation among Olea europaea fruit tissues in late development. Int. J. Mol. Sci. 21, 4819. doi: 10.3390/ijms21144819
Bures, M. S., Bandic, L. M., Vlahovicek-Kahlina, K. (2023). Determination of bioactive components in mandarin fruits: A review. Crit. Rev. Anal. Chem. 53, 1489–1514. doi: 10.1080/10408347.2022.2035209
Camarero, M. C., Briegas, B., Labrador, J., Gallardo, M., Gomez-Jimenez, M. C. (2023). Characterization of transcriptome dynamics during early fruit development in olive (Olea europaea L.). Int. J. Mol. Sci. 24, 961. doi: 10.3390/ijms24020961
Carey, S., Mendler, K., Hall, J. C. (2019). How to build a fruit: Transcriptomics of a novel fruit type in the Brassicaceae. PloS One 14, e0209535. doi: 10.1371/journal.pone.0209535
Cavalcante de Oliveira, A., Moreira Mar, J., Frota Corrêa, R., Sanches, E. A., Campelo, P. H., da Silva Ramos, A., et al. (2023). Pouteria spp. fruits: Health benefits of bioactive compounds and their potential for the food industry. Food Res. Int. 173, 113310. doi: 10.1016/j.foodres.2023.113310
Chen, K., Huang, G., Li, Y., Zhang, X., Lei, Y., Li, Y., et al. (2022). Illumina MiSeq sequencing reveals correlations among fruit ingredients, environmental factors, and AMF communities in three Lycium barbarum producing regions of China. Microbiol. Spectr. 10, e02293-21. doi: 10.1128/spectrum.02293-21
Cramer, G. R., Cochetel, N., Ghan, R., Destrac-Irvine, A., Delrot, S. (2020). A sense of place: Transcriptomics identifies environmental signatures in Cabernet Sauvignon berry skins in the late stages of ripening. BMC Plant Biol. 20, 41. doi: 10.1186/s12870-020-2251-7
Diao, Q., Tian, S., Cao, Y., Yao, D., Fan, H., Zhang, Y. (2023). Transcriptome analysis reveals association of carotenoid metabolism pathway with fruit color in melon. Sci. Rep. 13, 5004. doi: 10.1038/s41598-023-31432-y
Feng, G., Wu, J., Yi, H. (2019). Global tissue-specific transcriptome analysis of Citrus sinensis fruit across six developmental stages. Sci. Rep. 6, 153. doi: 10.1038/s41597-019-0162-y
Galla, G., Barcaccia, G., Ramina, A., Collani, S., Alagna, F., Baldoni, L., et al. (2009). Computational annotation of genes differentially expressed along olive fruit development. BMC Plant Biol. 9, 128. doi: 10.1186/1471-2229-9-128
Gao, X., Wang, L., Zhang, H., Zhu, B., Lv, G., Xiao, J. (2021). Transcriptome analysis and identification of genes associated with floral transition and fruit development in rabbiteye blueberry (Vaccinium ashei). PloS One 16, e0259119. doi: 10.1371/journal.pone.0259119
Gillaspy, G., Ben-David, H., Gruissem, W. (1993). Fruits: A developmental perspective. Plant Cell 5, 1439–1451. doi: 10.2307/3869794
Golovinskaia, O., Wang, C.-K. (2021). Review of functional and pharmacological activities of berries. Molecules 26, 3904. doi: 10.3390/molecules26133904
Gómez, M. D., Vera-Sirera, F., Pérez-Amador, M. A. (2014). Molecular programme of senescence in dry and fleshy fruits. J. Exp. Bot. 65, 4515–4526. doi: 10.1093/jxb/eru093
Gramzou, L., Klupsch, K., Fernández-Pozo, N., Höltzer, M., Marz, M., Rensing, S. A., et al. (2022). Comparative transcriptomics identifies candidate genes involved in the evolutionary transition from dehiscent to indehiscent fruits in Lepidium (Brasicaceae). BMC Plant Biol. 22, 340. doi: 10.1186/s12870-022-03631-8
Guo, C., Wei, Y., Yang, B., Ayup, M., Li, N., Liao, K., et al. (2021). Developmental transcriptome profiling uncovered carbon signaling genes associated with almond fruit drop. Sci. Rep. 11, 3401. doi: 10.1038/s41598-020-69395-z
Huang, G., Li, T., Li, X., Tan, D., Jiang, Z., Wei, Y., et al. (2014). Comparative transcriptome analysis of climacteric fruits of Chines pear (Pyrus ussuriensis) reveals new insights into fruit ripening. PloS One 9, e107562. doi: 10.1371/journal.pone.0107562
Huang, M., Zhu, X., Bai, H., Wang, C., Gou, N., Zhang, Y., et al. (2023). Comparative anatomical and transcriptomics reveal the larger cell size as a major contributor to larger fruit size in apricot. Int. J. Mol. Sci. 24, 8748. doi: 10.3390/ijms24108748
Kapoor, L., Simkin, A. J., Doss, G. P., Siva, R. (2022). Fruit ripening: dynamics and integrated analysis of carotenoids and anthocyanins. BMC Plant Biol. 22, 27. doi: 10.1186/s12870-021-03411-w
Karlova, R., Chapman, N., David, K., Angenent, G. C., Seymour, G. B., de Maagd, R. A. (2014). Transcriptional control of fleshy fruit development and ripening. J. Exp. Bot. 65, 4527–4541. doi: 10.1093/jxb/eru316
Kasampalis, D. S., Tsouvaltzis, P., Ntouros, K., Gertsis, A., Gitas, I., Moshou, D., et al. (2022). Nutritional composition changes in bell pepper as affected by the ripening stage of fruits at harvest or postharvest storage and assessed non-destructively. J. Sci. Food Agric. 102, 445–454. doi: 10.1002/jsfa.11375
Klee, H. J. (2010). Improving the flavor of fresh fruits: genomics, biochemistry, and biotechnology. New Phytol. 187, 44–56. doi: 10.1111/j.1469-8137.2010.03281.x
Koia, J. H., Moyle, R. L., Botella, J. R. (2012). Microarray analysis of gene expression profiles in ripening pineapple fruits. BMC Plant Biol. 12, 240. doi: 10.1186/1471-2229-12-240
Kou, X., Feng, Y., Yuan, S., Zao, X., Wu, C., Wang, C., et al. (2021). Different regulatory mechanisms of plant hormones in the ripening of climacteric and non-climacteric fruits: A review. Plant Mol. Biol. 107, 477–497. doi: 10.1007/s11103-021-01199-9
Lei, D., Lin, Y., Chen, Q., Zhao, B., Tang, H., Zhang, Y., et al. (2022). Transcriptomic analysis and the effect of maturity stage on fruit quality reveal the importance of the L- galactose pathway in the ascorbate biosynthesis of hardy kiwifruit (Actinidia arguta). Int. J. Mol. Sci. 23, 6816. doi: 10.3390/ijms23126816
Li, M., Galimba, K., Xiao, Y., Dardick, C., Mount, S. M., Callahan, A., et al. (2022). Comparative transcriptomic analysis of apple and peach fruits: Insights into fruit type specification. Plant J. 109, 1614–1629. doi: 10.1111/tpj.15633
Li, T., Wang, Y.-H., Liu, J.-X., Xu, Z.-S., Xion, A.-S. (2019). Advances in genomic, transcriptomic, proteomic, and metabolomic approaches to study biotic stress in fruit crops. Crit. Rev. Biotechnol. 39, 680–692. doi: 10.1080/07388551.2019.1608153
Li, D., Zand, M. S., Dye, T. D., Goniewicz, M. L., Rahman, I., Xie, Z. (2022). An evaluation of RNA-seq differential analysis methods. PloS One 17, e0264246. doi: 10.1371/journal.pone.0264246
Liu, W., Chen, M., Bai, L., Zhuang, Z., Fan, C., Jiang, N., et al. (2017). Comprehensive transcriptomics and proteomics analyses of pollinated and parthenocarpic litchi (Litchi chinensis Sonn.) fruits during early development. Sci. Rep. 7, 5401. doi: 10.1038/s41598-017-05724-z
Liu, H., Zhang, X., Li, J., Zhang, G., Fang, H., Li, Y. (2023). Transcriptome analysis reveals the mechanisms of different fruit appearance between apricot (Armeniaca vulgaris Lam.) and its seedlings. Mol. Biol. Rep. 50, 7995–8003. doi: 10.1007/s11033-023-08631-x
Luo, X., Cao, D., Li, H., Zhao, D., Xue, H., Niu, J., et al. (2018). Complementary iTRAQ-based proteomic and RNA sequencing-based transcriptomic analyses reveal a complex network regulating pomegranate (Punica granatum L.) fruit colour. Sci. Rep. 8, 12362. doi: 10.1038/s41598-018-30088-3
Martin, L. B. B., Nicolas, P., Matas, A. J., Shinozaki, Y., Catalá, C., Rose, J. K. (2016). Laser microdissection of tomato fruit cell and tissue types for transcriptome profiling. Nat. Protoc. 11, 2376–2388. doi: 10.1038/nprot.2016.146
Martínez, O., Arce-Rodríguez, M. L., Hernández-Godínez, F., Escoto-Sandoval, C., Cervantes-Hernández, F., Hayano-Kanashiro, C., et al. (2021). Transcriptome analyses throughout chili pepper fruits development reveal novel insights into the domestication process. Plants 10, 585. doi: 10.3390/plants10030585
Martínez-López, L. A., Ochoa-Alejo, N., Martínez, O. (2014). Dynamics of the chili pepper transcriptome during fruit development. BMC Genomics 15, 143. doi: 10.1186/1471-2164-15-143
McKee, L. H., Latner, T. A. (2000). Underutilized sources of dietary fiber: A review. Plant Foods Hum. Nutr. 55, 285–304. doi: 10.1023/A:1008144310986
Minio, A., Massonnet, M., Figueroa-Balderas, R., Vondras, A. M., Blanco-Ulate, B., Cantu, D. (2019). Iso-seq allows genome-independent transcriptome profiling of grape berry development. G3 Genes Genomes Genet. 9, 755–767. doi: 10.1534/g3.118.201008
Mizzotti, C., Rotasperti, L., Moretto, M., Tadini, L., Resentini, F., Galliani, B., et al. (2018). Time-course transcriptome analysis of Arabidopsis thaliana siliques discloses genes essential for fruit development and maturation. Plant Physiol. 178, 1249–1268. doi: 10.1104/pp.18.00727
Pandit, S. S., Kulkarni, R. S., Giri, A. P., Kölner, T. G., Degenhardt, J., Gershenzon, J., et al. (2010). Expression profiling of various genes during development and ripening of mango. Plant Physiol. Biochem. 48, 426–433. doi: 10.1016/j.plaphy.2010.02.012
Parra, R., Paredes, M. A., Sanchez-Calle, I. M., Gomez-Jimenez, M. C. (2013). Comparative transcriptional profiling analysis of olive ripe-fruit pericarp and abscission zone tissues shows expression differences and distinct patterns of transcriptional regulation. BMC Genomics 14, 866. doi: 10.1186/1471-2164-14-866
Qiao, H., Zhang, H., Wang, Z., Shen, Y. (2021). Fig fruit ripening is regulated by the interaction between ethylene and abscisic acid. J. Integr. Plant Biol. 63, 553–569. doi: 10.1111/jipb.13065
Rodríguez, A., Alquézar, B., Peña, L. (2012). Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal. New Phytol. 197, 36–48. doi: 10.1111/j.1469-8137.2012.04382.x
Romero, I., Escribano, M. I., Merodio, C., Sanchez-Ballesta, M. T. (2022). Postharvest high CO2 treatments on the quality of soft fruit berries: An integrated transcriptomic, proteomic, and metabolomic approach. J. Agric. Food Chem. 70, 8593–8597. doi: 10.1021/acs.jafc.2c01305
Roth, I. (1977). “Fruits of angiosperms,” in Encyclopedia of plant anatomy (Gebrüder Borntraeger, Berlin, Stuttgart), 675.
Saladié, M., Cañizares, J., Phillips, M. A., Rodriguez-Concepcion, M., Larrigaudière, C., Gibon, Y., et al. (2015). Comparative transcriptional profiling analysis of developing melon (Cucumis melo L.) fruit from climacteric and non-climacteric varieties. BMC Genomics 16, 440. doi: 10.1186/s12864-015-1649-3
Seymour, G. B., Østergaard, L., Chapman, N. H., Knapp, S., Martin, C. (2013). Fruit development and ripening. Annu. Rev. Plant Biol. 64, 219–241. doi: 10.1146/annurev-arplant-050312-120057
Seymour, G., Poole, M., Manning, K., King, G. J. (2008). Genetics and epigenetics of fruit development and ripening. Curr. Opin. Plant Biol. 11, 58–63. doi: 10.1016/j.pbi.2007.09.003
Shi, S., Li, D., Li, S., Wang, Y., Tang, X., Liu, Y., et al. (2023). Comparative transcriptomic analysis of early development in eggplant (Solanum melongena L.) and functional characterization of SmOvate5. Plant Cell Rep. 42, 321–336. doi: 10.1007/s00299-022-02959-7
Shinozaki, Y., Nicolas, P., Fernandez-Pozo, N., Ma, Q., Evanich, D. J., Shi, Y., et al. (2018). High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening. Nat. Commun. 9, 363. doi: 10.1038/s41467-017-02782-9
Stournaras, K. E., Lo, E., Böhning-Gaese, K., Cazzeta, E., Dehling, D. M., Schleuning, M., et al. (2012). How colorful are fruits? Limited color diversity in fleshy fruits on local and global scales. New Phytol. 198, 617–629. doi: 10.1111/nph.12157
Tafolla-Arellano, J. C., Zheng, Y., Sun, H., Jiao, C., Ruiz-May, C., Hernandez-Oñate, A., et al. (2017). Transcriptome analysis of mango (Mangifera indica L.) fruit epidermal peel to identify putative cuticle-associated genes. Sci. Rep. 7, 46163. doi: 10.1038/srep46163
Tang, N., Deng, W., Hu, G., Hu, N., Li, Z. (2015). Transcriptome profiling reveals the regulatory mechanism underlying pollination dependent and parthenocarpic fruit set mainly mediated by auxin and gibberellin. PloS One 10, e0125355. doi: 10.1371/journal.pone.0125355
Tarazona, S., García-Alcalde, F., Dopazo, J., Ferrer, A., Conesa, A. (2011). Differential expression in RNA-seq: A matter of depth. Genome Res. 21, 2213–2223. doi: 10.1101/gr.124321.111
Trapnell, C., Hendrickson, D. G., Sauvageau, M., Goff, L., Rinn, J. L., Pachter, L. (2013). Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31, 46–53. doi: 10.1038/nbt.2450
Tsaballa, A., Pasentsis, K., Darzentas, N., Tsaftaris, A. S. (2011). Multiple evidence for the role of an Ovate-like gene in determining fruit shape in pepper. BMC Plant Biol. 11, 46. doi: 10.1186/1471-2229-11-46
Van de Poel, B., Bulens, I., Hertog, M. L. A. T. M., Nicolai, B. M., Geeraerd, A. H. (2014). A transcriptomics-based kinetic model for ethylene biosynthesis in tomato (Solanum lycopersicum) fruit: Development, validation and exploration of novel regulatory mechanisms. New Phytol. 202, 952–963. doi: 10.1111/nph.12685
Velculescu, V. E., Zhang, L., Zhou, W., Vogelstein, J., Basrai, M. A., Bassett, D. E., et al. (1997). Characterization of the yeast transcriptome. Cell 88, 243–251. doi: 10.1016/S0092-8674(00)81845-0
Villa-Rivera, M. G., Martínez, O., Ochoa-Alejo, N. (2022). Putative transcription factor genes associated with regulation of carotenoid biosynthesis in chili pepper fruits revealed by RNA-Seq coexpression analysis. Int. J. Mol. Sci. 23, 11774. doi: 10.3390/ijms231911774
Waite, J. M., Kelly, E. A., Zhang, H., Hargarten, H. L., Waliullah, S., Altman, N. S., et al. (2023). Transcriptomic approach to uncover dynamic events in the development of mid-season sunburn in apple fruit. G3 13, jkad120. doi: 10.1093/g3journal/jkad120
Wang, L., Chen, Y., Wang, S., Xue, H., Su, Y., Yang, J., et al. (2018). Identification of candidate genes involved in the sugar metabolism and accumulation during pear fruit post-harvest ripening of ‘Red Clapps’s Favorite (Pyrus communis L.) by transcriptomic analysis. Hereditas 155, 11. doi: 10.1186/s41065-017-0046-0
Wang, Z., Gerstein, M., Snyder, M. (2009). RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10, 57–63. doi: 10.1038/nrg2484
Wu, Y., Xu, J., He, Y., Shi, M., Han, X., Li, W., et al. (2019). Metabolic profiling of pitaya (Hylocereus polyrhizus) during fruit development and maturation. Molecules 24, 1114. doi: 10.3390/molecules24061114
Wu, S., Zhang, B., Keyhaninejad, N., Rodríguez, G. R., Kim, H. J., Chakrabarti, M., et al. (2018). A common genetic mechanism underlies morphological diversity in fruits and other plant organs. Nat. Commun. 9, 4734. doi: 10.1038/s41467-018-07216-8
Xie, M., Huang, Y., Zhang, Y., Wang, X., Yang, H., Yu, O., et al. (2013). Transcriptome profiling of fruit development and maturation in Chinese white pear (Pyrus bretschneideri Rehd). BMC Genomics 14, 823. doi: 10.1186/1471-2164-14-823
Xu, J., Yan, J., Li, W., Wang, Q., Wang, C., Guo, J., et al. (2020). Integrative analyses of widely targeted metabolic profiling and transcriptome data reveals molecular insight into metabolomic variations during apple (Malus domestica) fruit development and ripening. Int. J. Mol. Sci. 21, 4797. doi: 10.3390/ijms21134797
Yang, L., Liu, L., Wang, Z., Zong, Y., Yu, L., Li, Y., et al. (2021). Comparative anatomical and transcriptomic insights into Vaccinium corymbosum flower bud and fruit throughout development. BMC Plant Biol. 21, 289. doi: 10.1186/s12870-021-03067-6
Yang, H., Tian, C., Ji, S., Ni, F., Fan, X., Yang, Y., et al. (2021). Integrative analyses of metabolome and transcriptome reveals metabolomic variations and candidate genes involved in sweet cherry (Prunus avium L.) fruit quality during development and ripening. PloS One 16, e0260004. doi: 10.1371/journal.pone.0260004
Ye, J., Hu, T., Yang, C., Li, H., Yang, M., Ijaz, R., et al. (2015). Transcriptome profiling of tomato fruit development reveals transcription factors associated with ascorbic acid, carotenoid and flavonoid biosynthesis. PloS One 10, e0130885. doi: 10.1371/journal.pone.0130885
Yu, X., Ali, M. M., Li, B., Fang, T., Chen, F. (2021). Transcriptome data-based identification of candidate genes involved in metabolism and accumulation of soluble sugars during fruit development in ‘Huangguan’ plum. J. Food Biochem. 45, e13878. doi: 10.1111/jfbc.13878
Yun, D., Yan, Y., Liu, J. (2022). Isolation, structure and biological activity of polysaccharides from fruits of Lycium ruthenicum Murr.: A review. Carbohyd. Polym. 291, 119618. doi: 10.1016/j.carbpol.2022.119618
Zamora, R., Alaiz, M., Hidalgo, F. J. (2001). Influence of cultivar and fruit ripening on olive (Olea europaea) fruit protein content, composition, and antioxidative activity. J. Agric. Food Chem. 49, 4267–4270. doi: 10.1021/jf0104634
Zhang, M.-Y., Xue, C., Xu, L., Sun, H., Qin, M.-F., Zhang, S., et al. (2016). Distinct transcriptome profiles reveal gene expression patterns during fruit development and maturation in five main cultivated species of pear (Pyrus L.). Sci. Rep. 6, 28130. doi: 10.1038/srep28130
Zhang, A., Zheng, J., Chen, X., Shi, X., Wang, H., Fu, Q. (2021). Comprehensive analysis of transcriptome and metabolome reveals the flavonoid metabolic pathway is associated with fruit peel coloration of melon. Molecules 26, 2830. doi: 10.3390/molecules26092830
Zhao, J., Li, H., Yin, Y., An, W., Qin, X., Wang, Y., et al. (2020). Transcriptomic and metabolomic analyses of Lycium ruthenicum and Lycium barbarum fruits during ripening. Sci. Rep. 10, 4354. doi: 10.1038/s41598-020-61064-5
Zhou, J., Li, M., Li, Y., Xiao, Y., Luo, X., Gao, S., et al. (2023). Comparison of red raspberry and wild strawberry fruits reveals mechanisms of fruit type specification. Plant Physiol. 193, 1016–1035. doi: 10.1093/plphys/kiad409
Zhou, X., Liu, S., Yang, Y., Liu, J., Zhuang, Y. (2022). Integrated metabolome and transcriptome analysis reveals a regulatory network of fruit peel pigmentation in eggplant (Solanum melongena L.). Int. J. Mol. Sci. 23, 13475. doi: 10.3390/ijms232113475
Zhu, H., Dardick, C. D., Beers, E. P., Callanhan, A. M., Xia, R., Yuan, R. (2011). Transcriptomics of shading-induced and NAA-induced abscission in apple (Malus domestica) reveals a shared pathway involving reduced photosynthesis, alterations in carbohydrate transport and signaling and hormone cross-talk. BMC Plant Biol. 11, 138. doi: 10.1186/1471-2229-11-138
Keywords: carbamoyltransferases, carotenoids, core genes, flavor, fruit, histone acetyltransferases, metabolomics, regulatory network
Citation: Ochoa-Alejo N, Gómez-Jiménez MC and Martínez O (2024) Editorial: Transcriptomics of fruit growth, development and ripening. Front. Plant Sci. 15:1399376. doi: 10.3389/fpls.2024.1399376
Received: 11 March 2024; Accepted: 27 March 2024;
Published: 05 April 2024.
Edited and Reviewed by:
Neelima Roy Sinha, University of California, Davis, United StatesCopyright © 2024 Ochoa-Alejo, Gómez-Jiménez and Martínez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Neftali Ochoa-Alejo, bmVmdGFsaS5vY2hvYUBjaW52ZXN0YXYubXg=