Abstract
Main conclusion
Gene expression variations in response to fertilization between Physalis and Solanum might play essential roles in species divergence and fruit evolution.
Abstract
Fertilization triggers variation in fruit development and morphology. The Chinese lantern, a morphological novelty derived from the calyx, is formed upon fertilization in Physalis but is not observed in Solanum. The underlying genetic variations are largely unknown. Here, we documented the developmental and morphological differences in the flower and fruit between Physalis floridana and Solanum pimpinellifolium and then evaluated both the transcript sequence variation and gene expression at the transcriptomic level at fertilization between the two species. In Physalis transcriptomic analysis, 468 unigenes were identified as differentially expressed genes (DEGs) that were strongly regulated by fertilization across 3 years. In comparison with tomato, 14,536 strict single-copy orthologous gene pairs were identified between P. floridana and S. pimpinellifolium in the flower–fruit transcriptome. Nine types of gene variations with specific GO-enriched patterns were identified, covering 58.82% orthologous gene pairs that were DEGs in either trend or dosage at the flower–fruit transition between the two species, which could adequately distinguish Solanum and Physalis, implying that differential gene expression at fertilization might play essential roles during the divergence and fruit evolution of Solanum–Physalis. Virus-induced gene silencing analyses revealed the developmental roles of some transcription factor genes in fertility, Chinese lantern development, and fruit weight control in Physalis. This study presents the first floral transcriptomic resource of Physalis, and reveals some candidate genetic variations accounting for the early fruit developmental evolution in Physalis in comparison to Solanum.
Similar content being viewed by others
Data availability
All relevant supporting data can be found within the additional files accompanying this article. The RNA-Seq reads described in the article were deposited at the Sequence Read Archive (SRA) database under the accession number PRJNA552437.
Abbreviations
- DEG:
-
Differentially expressed gene
- GO:
-
Gene ontology
- ICS:
-
Inflated calyx syndrome
- PCA:
-
Principal component analysis
- TF:
-
Transcription factor
- VIGS:
-
Virus-induced gene silencing
References
Auer PL, Doerge RW (2010) Statistical design and analysis of RNA sequencing data. Genetics 185(2):405–416
Brawand D, Soumillon M, Necsulea A, Julien P, Csárdi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, Albert FW, Zeller U, Khaitovich P, Grützner F, Bergmann S, Nielsen R, Pääbo S, Kaessmann H (2011) The evolution of gene expression levels in mammalian organs. Nature 478:343–348
Chakrabarti M, Zhang N, Sauvage C, Muños S, Blanca J, Cañizares J, Diez MJ, Schneider R, Mazourek M, McClead J, Causse M, van der Knaap E (2013) A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci USA 11:17125–17130
Cong B, Barrero LS, Tanksley SD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804
Dafni A, Maués MM (1998) A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod 11:177–180
Doebley J, Lukens L (1998) Transcriptional regulators and the evolution of plant form. Plant Cell 10:1075–1082
Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321
Dresselhaus T, Sprunck S, Wessel GM (2016) Fertilization mechanisms in flowering plants. Curr Biol 26:R125–R139
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
Fulton TM, Van der Hoeven R, Eannetta NT, Tanksley SD (2002) Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14:1457–1467
Gazón-Martínez GA, Zhu Z, Landsman D, Barrero LS, Mariño-Ramírez L (2012) The Physalis peruviana leaf transcriptome: assembly, annotation and gene model prediction. BMC Genomics 13:151–163
Grabherr MG, Has BJ, Yassour M, Levin JZ, Thompson DA, AmitI AX, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
Han X, Shen T, Lou H (2007) Dietary polyphenols and their biological significance. Int J Mol Sci 8:950–988
Hassanien MFR (2011) Physalis peruviana: a rich source of bioactive phytochemicals for functional foods and pharmaceuticals. Food Rev Int 27:259–273
He CY, Saedler H (2005) Heterotopic expression of MPF2 is the key to the evolution of the Chinese lantern of Physalis, a morphological novelty in Solanaceae. Proc Natl Acad Sci USA 102:5779–5784
He CY, Saedler H (2007) Hormonal control of the inflated calyx syndrome, a morphological novelty, in Physalis. Plant J 49:935–946
He CY, Münster T, Saedler H (2004) On the origin of floral morphological novelties. FEBS Lett 567:147–151
He CY, Tian Y, Saedler R, Efremova N, Riss S, Khan MR, Yephremov A, Saedler H (2010) The MADS-domain protein MPF1 of Physalis floridana controls plant architecture, seed development and flowering time. Planta 231:767–777
He H, Zang L, Feng Y, Wang J, Liu W, Chen L, Kang N, Tashiro S, Onodera S, Qiu F, Ikejima T (2013) Physalin A induces apoptotic cell death and protective autophagy in HT1080 human fibrosarcoma cells. J Nat Prod 76:880–888
Huang B, Routaboul JM, Liu M, Deng W, Maza E, Mila I, Hu G, Zouine M, Frasse P, Vrebalov JT, Giovannoni JJ, Li Z, van der Rest B, Bouzayen M (2017) Overexpression of the class D MADS-box gene Sl-AGL11 impacts fleshy tissue differentiation and structure in tomato fruits. J Exp Bot 68:4869–4884
Ichihashi Y, Aguilar-Martínez JA, Farhi M, Chitwood DH, Kumar R, Millon LV, Peng J, Maloof JN, Sinha NR (2014) Evolutionary developmental transcriptomics reveals a gene network module regulating interspecific diversity in plant leaf shape. Proc Natl Acad Sci USA 111:2616–2621
Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 7:138–148
Ji L, Yuan Y, Luo L, Chen Z, Ma X, Ma Z, Cheng L (2012) Physalins with anti-inflammatory activity are present in Physalis alkekengi var. franchetii and can function as Michael reaction acceptors. Steroids 77:441–447
Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022
Knapp S, Bohs L, Nee M, Spooner DM (2004) Solanaceae - a model for linking genomics with biodiversity. Comp Funct Genom 5:285–291
Koenig D, Jimenez-Gomez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumar R, Covington MF, Devisetty UK, Tat AV, Tohge T, Bolger A, Schneeberger K, Ossowski S, Lanz C, Xiong G, Taylor-Teeples M, Brady SM, Pauly M, Weigel D, Usadel B, Fernie AR, Peng J, Sinha NR, Maloof JN (2013) Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci USA 110:E2655–2662
Lemmon ZH, Reem NT, Dalrymple J, Soyk S, Swartwood KE, Rodriguez-Leal D, Van Eck J, Lippman ZB (2018) Rapid improvement of domestication traits in an orphan crop by genome editing. Nat Plants 4:766–770
Li Z, He CY (2015) Physalis floridana Cell Number Regulator1 encodes a cell membrane-anchored modulator of cell cycle and negatively controls fruit size. J Exp Bot 66:257–270
Li L, Stoeckert CJ, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189
Li T, Yang X, Yu Y, Si X, Zhai X, Zhang H, Dong W, Gao C, Xu C (2018) Domestication of wild tomato is accelerated by genome editing. Nat Biotechnol 36:1160–1163
Li J, Song CJ, He CY (2019) Chinese lantern in Physalis is an advantageous morphological novelty and improves plant fitness. Sci Rep 9:596
Liu J, VanEck J, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear shaped tomato fruit. Proc Natl Acad Sci USA 99:13302–13306
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔ CT method. Methods 25:402–408
Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, Tohge T, Ponnala L, Adato A, Aharoni A, Stark R, Fernie AR, Fei Z, Giovannoni JJ, Rose JK (2011) Tissue- and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 23:3893–3910
Matsuura T, Kawai M, Makashima R, Butsugan Y (1970) Structures of physalin A and physalin B, 13,14-seco-16,24-cyclo-steroids from Physalis alkekengi var. Franchetii. J Chem Soc C Org 5:664–670
Mu Q, Huang Z, Chakrabarti M, Illa-Berenguer E, Liu X, Wang Y, Ramos A, van der Knaap E (2017) Fruit weight is controlled by Cell Size Regulator encoding a novel protein that is expressed in maturing tomato fruits. PLoS Genet 13:e1006930
Muños S, Ranc N, Botton E, Bérard A, Rolland S, Duffé P, Carretero Y, Le Paslier MC, Delalande C, Bouzayen M, Brunel D, Causse M (2011) Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 156:2244–2254
Pattison RJ, Csukasi F, Zheng Y, Fei Z, van der Knaap E, Catalá C (2015) Comprehensive tissue-specific transcriptome analysis reveals distinct regulatory programs during early tomato fruit development. Plant Physiol 168:1684–1701
Peng S, Jiang H, Zhang S, Chen L, Li X, Korpelainen H, Li C (2012) Transcriptional profiling reveals sexual differences of the leaf transcriptomes in response to drought stress in Populus yunnanensis. Tree Physiol 32:1541–1555
Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1:66–69
Purugganan MD, Fuller DQ (2009) The nature of selection during plant domestication. Nature 457:843–848
Qiu L, Zhao F, Jiang Z, Chen L, Zhao Q, Liu H, Yao X, Qiu F (2008) Steroids and flavonoids from Physalis alkekengi var. franchetii and their inhibitory effects on nitric oxide production. J Nat Prod 1:642–646
Rensing SA (2014) Gene duplication as a driver of plant morphogenetic evolution. Curr Opin Plant Biol 17:43–48
Robles JA, Qureshi SE, Stephen SJ, Wilson SR, Burden CJ, Taylor JM (2012) Efficient experimental design and analysis strategies for the detection of differential expression using RNA-Sequencing. BMC Genomics 13:484
Roux J, Rosikiewicz M, Robinson-Rechavi M (2015) What to compare and how: comparative transcriptomics for Evo-Devo. J Exp Zool B Mol Dev Evol 324:372–382
Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378
Sun S, Zhou Y, Chen J, Shi J, Zhao H, Zhao H, Song W, Zhang M, Cui Y, Dong X, Liu H, Ma X, Jiao Y, Wang B, Wei X, Stein JC, Glaubitz JC, Lu F, Yu G, Liang C, Fengler K, Li B, Rafalski A, Schnable PS, Ware DH, Buckler ES, Lai J (2018) Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nat Genet 50:1289–1295
Swanson-Wagner R, Briskine R, Schaefer R, Hufford MB, Ross-Ibarra J, Myers CL, Tiffin P, Springer NM (2012) Reshaping of the maize transcriptome by domestication. Proc Natl Acad Sci USA 109:11878–11883
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tarazona S, Furió-Tarí P, Turrà D, Pietro AD, Nueda MJ, Ferrer A, Conesa A (2015) Data quality aware analysis of differential expression in RNA-seq with NOISeq R/Bioc package. Nucleic Acids Res 43(21):e140
The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195
Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85
Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515
Wang L, He L, Li J, Zhao J, Li Z, He CY (2014) Regulatory change at Physalis Organ Size 1 correlates to natural variation in tomatillo reproductive organ size. Nat Commun 5:4271
Wang L, Li J, Zhao J, He CY (2015) Evolutionary developmental genetics of fruit morphological variation within the Solanaceae. Front Plant Sci 6:248
Wittkopp PJ, Kalay G (2011) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69
Wray GA (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8:206–216
Wu F, Mueller LA, Crouzillat D, Pétiard V, Tanksley SD (2006) Combining bioinformatics and phylogenetics to identify large sets of single-copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the euasterid plant clade. Genetics 174:1407–1420
Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008) A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319:1527–1530
Xu J, Sun J, Du L, Liu X (2012a) Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytol 196:110–124
Xu M, Cho E, Burch-Smith TM, Zambryski PC (2012b) Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis. Proc Natl Acad Sci USA 109:5098–5103
Xu C, Liberatore KL, Macalister CA, Huang Z, Chu YH, Jiang K, Brooks C, Ogawa-Ohnishi M, Xiong G, Pauly M, Van Eck J, Matsubayashi Y, van der Knaap E, Lippman ZB (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47:784–792
Yang Z (2007) PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol 152:1787–1795
Zhang J, Zhao J, Zhang S, He CY (2014) Efficient gene silencing mediated by tobacco rattle virus in an emerging model plant Physalis. PLoS ONE 9:e85534
Zhao J, Tian Y, Zhang J, Zhao M, Gong P, Riss S, Saedler R, He CY (2013) The euAP1 protein MPF3 represses MPF2 to specify floral calyx identity and displays crucial roles in Chinese lantern development in Physalis. Plant Cell 25:2002–2021
Zsögön A, Čermák T, Naves ER, Notini MM, Edel KH, Weinl S, Freschi L, Voytas DF, Kudla J, Peres LEP (2018) De novo domestication of wild tomato using genome editing. Nat Biotechnol 36:1211–1216
Acknowledgements
We appreciate Drs PC Gong and J Zhao for their assistances respectively in photograph under microscope, pollen staining and VIGS analyses.
Funding
This work was supported by grants from the National Natural Science Foundation of China (31525003 and 91331103) and by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB27010106).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gao, H., Li, J., Wang, L. et al. Transcriptomic variation of the flower–fruit transition in Physalis and Solanum. Planta 252, 28 (2020). https://doi.org/10.1007/s00425-020-03434-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03434-x