Deciphering the evolutionary development of the "Chinese lantern" within Solanaceae.
Physalis
Evo-devo
ICS
MADS-box gene
Morphological novelty
Origin
Journal
Planta
ISSN: 1432-2048
Titre abrégé: Planta
Pays: Germany
ID NLM: 1250576
Informations de publication
Date de publication:
18 Sep 2024
18 Sep 2024
Historique:
received:
27
05
2024
accepted:
15
09
2024
medline:
18
9
2024
pubmed:
18
9
2024
entrez:
18
9
2024
Statut:
epublish
Résumé
The key genetic variation underlying the evo-devo of ICS in Solanaceae may be further pinpointed using an integrated strategy of forward and reverse genetics studies under the framework of phylogeny. The calyx of Physalis remains persistent throughout fruit development. Post-flowering, the fruiting calyx is inflated rapidly to encapsulate the berry, giving rise to a "Chinese lantern" structure called inflated calyx syndrome (ICS). It is unclear how this novelty arises. Over the past 2 decades, the role of MADS-box genes in the evolutionary development (evo-devo) of ICS has mainly been investigated within Solanaceae. In this review, we analyze the main achievements, challenges, and new progress. ICS acts as a source for fruit development, provides a microenvironment to protect fruit development, and assists in long-distance fruit dispersal. ICS is a typical post-floral trait, and the onset of its development is triggered by specific developmental signals that coincide with fertilization. These signals can be replaced by exogenous gibberellin and cytokinin application. MPF2-like heterotopic expression and MBP21-like loss have been proposed to be two essential evolutionary events for ICS origin, and manipulating the related MADS-box genes has been shown to affect the ICS size, sepal organ identity, and/or male fertility, but not completely disrupt ICS. Therefore, the core genes or key links in the ICS biosynthesis pathways may have undergone secondary mutations during evolution, or they have not yet been pinpointed. Recently, we have made some encouraging progress in acquiring lantern mutants in Physalis floridana. In addition to technological innovation, we propose an integrated strategy to further analyze the evo-devo mechanisms of ICS in Solanaceae using forward and reverse genetics studies under the framework of phylogeny.
Identifiants
pubmed: 39292428
doi: 10.1007/s00425-024-04535-7
pii: 10.1007/s00425-024-04535-7
doi:
Substances chimiques
MADS Domain Proteins
0
Plant Proteins
0
Gibberellins
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
98Subventions
Organisme : the National Natural Science Foundation of China
ID : 32221001
Organisme : the National Natural Science Foundation of China
ID : 31930007
Organisme : the National Natural Science Foundation of China
ID : 31525003
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178
pubmed: 22267009
doi: 10.1038/nbt.2095
Arthur W (2002) The emerging conceptual framework of evolutionary developmental biology. Nature 415:757–764
pubmed: 11845200
doi: 10.1038/415757a
Azpiroz-Leehan R, Feldmann KA (1997) T-DNA insertion mutagenesis in Arabidopsis: going back and forth. Trends Genet 13:152–156
pubmed: 9097726
doi: 10.1016/S0168-9525(97)01094-9
Castañeda L, Giménez E, Pineda B, García-Sogo B, Ortiz-Atienza A, Micol-Ponce R, Angosto T, Capel J, Moreno V, Yuste-Lisbona FJ, Lozano R (2022) Tomato CRABS CLAW paralogues interact with chromatin remodelling factors to mediate carpel development and floral determinacy. New Phytol 234:1059–1074
pubmed: 35170044
pmcid: 9314824
doi: 10.1111/nph.18034
Clark JW (2023) Genome evolution in plants and the origins of innovation. New Phytol 240:2204–2209
pubmed: 37658677
doi: 10.1111/nph.19242
Deanna R, Larter MD, Barboza GE, Smith SD (2019) Repeated evolution of a morphological novelty: a phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae). Am J Bot 106:270–279
pubmed: 30779447
doi: 10.1002/ajb2.1242
Deanna R, Wilf P, Gandolfo MA (2020) New physaloid fruit-fossil species from early Eocene South America. Am J Bot 107:1749–1762
pubmed: 33247843
doi: 10.1002/ajb2.1565
Eisenstein M (2022) Seven technologies to watch in 2022. Nature 601:658–661
pubmed: 35079149
doi: 10.1038/d41586-022-00163-x
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:e19379
pubmed: 21573248
pmcid: 3087801
doi: 10.1371/journal.pone.0019379
Fu Y, Xiao W, Tian L, Guo L, Ma G, Ji C, Huang Y, Wang H, Wu X, Yang T, Wang J, Wang J, Wu Y, Wang W (2023) Spatial transcriptomics uncover sucrose post-phloem transport during maize kernel development. Nat Commun 14:7191
pubmed: 37938556
pmcid: 10632454
doi: 10.1038/s41467-023-43006-7
Gong PC, Song CJ, Liu HY, Li PG, Zhang MS, Zhang JS, Zhang SH, He CY (2021) Physalis floridana CRABS CLAW mediates neofunctionalization of GLOBOSA genes in carpel development. J Exp Bot 72:6882–6903
pubmed: 34181715
pmcid: 8547157
doi: 10.1093/jxb/erab309
Griesmann M, Chang Y, Liu X et al (2018) Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science 361:eaat1743
pubmed: 29794220
doi: 10.1126/science.aat1743
Han JJ, Jackson D, Martienssen R (2012) Pod corn is caused by rearrangement at the Tunicate1 locus. Plant Cell 24:2733–2744
pubmed: 22829149
pmcid: 3426111
doi: 10.1105/tpc.112.100537
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
pubmed: 15824316
pmcid: 556287
doi: 10.1073/pnas.0501877102
He CY, Saedler H (2007a) Hormonal control of the inflated calyx syndrome, a morphological novelty in Physalis. Plant J 49:935–946
pubmed: 17316177
doi: 10.1111/j.1365-313X.2006.03008.x
He CY, Saedler H (2007b) Molecular evolution of a morphological novelty in Solanaceae: the Inflated-Calyx-Syndrome (ICS) in Physalis. Acta Hort 745:171–182
doi: 10.17660/ActaHortic.2007.745.6
He CY, Münster T, Saedler H (2004) On the origin of floral morphological novelties. FEBS Lett 567:147–151
pubmed: 15165908
doi: 10.1016/j.febslet.2004.02.090
He CY, Sommer H, Grosardt B, Huijser P, Saedler H (2007) PFMAGO, a MAGO NASHI-like factor, interacts with the MADS-domain protein MPF2 from Physalis floridana. Mol Biol Evol 24:1229–1241
pubmed: 17339635
doi: 10.1093/molbev/msm041
He J, Alonge M, Ramakrishnan S, Benoit M, Soyk S, Reem NT, Hendelman A, Van Eck J, Schatz MC, Lippman ZB (2023) Establishing Physalis as a Solanaceae model system enables genetic reevaluation of the inflated calyx syndrome. Plant Cell 35:351–368
pubmed: 36268892
doi: 10.1093/plcell/koac305
Hu JY, Saedler H (2007) Evolution of the inflated calyx syndrome in Solanaceae. Mol Biol Evol 24:2443–2453
pubmed: 17827172
doi: 10.1093/molbev/msm177
Huerga-Fernández S, Detry N, Orman-Ligeza B, Bouché F, Hanikenne M, Périlleux C (2024) JOINTLESS maintains inflorescence meristem identity in tomato. Plant Cell Physiol 65:1197–1211
pubmed: 38635460
pmcid: 11287206
doi: 10.1093/pcp/pcae046
Jung C, Till B (2021) Mutagenesis and genome editing in crop improvement: perspectives for the global regulatory landscape. Trends Plant Sci 26:1258–1269
pubmed: 34465535
doi: 10.1016/j.tplants.2021.08.002
Khan MR, Hu JY, Riss S, He CY, Saedler H (2009) MPF2-like-A MADS-box genes control the inflated calyx syndrome in Withania (Solanaceae): roles of Darwinian selection. Mol Biol Evol 26:2463–2473
pubmed: 19608636
doi: 10.1093/molbev/msp159
Khan MR, Hu JY, He CY (2012) Plant hormones including ethylene are recruited in calyx inflation in Solanaceous plants. J Plant Physiol 169:940–948
pubmed: 22551956
doi: 10.1016/j.jplph.2012.02.015
Khan MR, Ihsan H, Ali GM (2016) WSA206, a paralog of duplicated MPF2-like MADS-box family is recruited in fertility function in Withania. Plant Sci 253:215–228
pubmed: 27968991
doi: 10.1016/j.plantsci.2016.10.004
Lebedeva M, Komakhin R, Konovalova L, Ivanova L, Taranov V, Monakhova Y, Babakov A, Klepikova A, Zlobin N (2022) Development of potato (Solanum tuberosum L.) plants with StLEAFY knockout. Planta 256:116
pubmed: 36374358
doi: 10.1007/s00425-022-04032-9
Lemmon ZH, Park SJ, Jiang K, Van Eck J, Schatz MC, Lippman ZB (2016) The evolution of inflorescence diversity in the nightshades and heterochrony during meristem maturation. Genome Res 26:1676–1686
pubmed: 27821409
pmcid: 5131819
doi: 10.1101/gr.207837.116
Li Z, Zeng S, Li Y, Li M, Souer E (2016) Leaf-like sepals induced by ectopic expression of a SHORT VEGETATIVE PHASE (SVP)-like MADS-box gene from the basal eudicot Epimedium sagittatum. Front Plant Sci 7:1461
pubmed: 27733858
pmcid: 5039176
Li J, Song CJ, He CY (2019) Chinese lantern in Physalis is an advantageous morphological novelty and improves plant fitness. Sci Rep 9:596
pubmed: 30679462
pmcid: 6345875
doi: 10.1038/s41598-018-36436-7
Li Z, Chen X, Shi S, Zhang H, Wang X, Chen H, Li W, Li L (2022) DeepBSA: a deep-learning algorithm improves bulked segregant analysis for dissecting complex traits. Mol Plant 15:1418–1427
pubmed: 35996754
doi: 10.1016/j.molp.2022.08.004
Liang Y, Liang L, Shi R, Luo R, Yue Y, Yu J, Wang X, Lin J, Zhou T, Yang M, Zhong L, Wang Y, Shu Z (2024) Genus Physalis L.: a review of resources and cultivation, chemical composition, pharmacological effects and applications. J Ethnopharmacol 24:117736
doi: 10.1016/j.jep.2024.117736
Lönnig WE (2010) Mutagenesis in Physalis pubescens L. ssp. floridana: some further research on Dollo’s law and the law of recurrent variation. Floric Ornam Biotechnol 4:1–21
Lu JJ, Luo MF, Wang L, Li KP, Yu YY, Yang WF, Gong PC, Gao HH, Li QR, Zhao J, Wu LF, Zhang MS, Liu XY, Zhang XM, Zhang X, Kang JY, Yu TY, Li ZM, Jiao YN, Wang HZ, He CY (2021) The Physalis floridana genome provides insights into the biochemical and morphological evolution of Physalis fruits. Hortic Res 8:244
pubmed: 34795210
pmcid: 8602270
doi: 10.1038/s41438-021-00705-w
Monniaux M, Vandenbussche M (2023) Flower development in the Solanaceae. Methods Mol Biol 2686:39–58
pubmed: 37540353
doi: 10.1007/978-1-0716-3299-4_2
Moyroud E, Glover BJ (2017) The evolution of diverse floral morphologies. Curr Biol 27:R941–R951
pubmed: 28898667
doi: 10.1016/j.cub.2017.06.053
Pantalacci S, Sémon M (2015) Transcriptomics of developing embryos and organs: a raising tool for evo–devo. J Exp Zool B Mol Dev Evo 324:363–371
doi: 10.1002/jez.b.22595
Pretz C, Deanna R (2020) Typifications and nomenclatural notes in Physalis (Solanaceae) from the United States. Taxon 69:170–192
doi: 10.1002/tax.12159
Qin C, Yu C, Shen Y et al (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. Proc Natl Acad Sci USA 111:5135–5140
pubmed: 24591624
pmcid: 3986200
doi: 10.1073/pnas.1400975111
Richman AD, Kohn JR (1999) Self-incompatibility alleles from Physalis: implications for historical inference from balanced genetic polymorphisms. Proc Natl Acad Sci USA 96:168–172
pubmed: 9874790
pmcid: 15111
doi: 10.1073/pnas.96.1.168
Scheben A, Batley J, Edwards D (2017) Genotyping-by-sequencing approaches to characterize crop genomes: choosing the right tool for the right application. Plant Biotechnol J 15:149–161
pubmed: 27696619
pmcid: 5258866
doi: 10.1111/pbi.12645
Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C (2013) Fruit development and ripening. Annu Rev Plant Biol 64:219–241
pubmed: 23394500
doi: 10.1146/annurev-arplant-050312-120057
Shenstone E, Lippman Z, Van Eck J (2020) A review of nutritional properties and health benefits of Physalis species. Plant Foods Hum Nutr 75:316–325
pubmed: 32385801
doi: 10.1007/s11130-020-00821-3
Tan Y, Li S (2022) Generation of mutants by combined treatment of physical and chemical mutagens in rice. Methods Mol Biol 2484:137–142
pubmed: 35461450
doi: 10.1007/978-1-0716-2253-7_11
Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641
doi: 10.1038/nature11119
Tung CC, Kuo SC, Yang CL, Yu JH, Huang CE, Liou PC, Sun YH, Shuai P, Su JC, Ku C, Lin YJ (2023) Single-cell transcriptomics unveils xylem cell development and evolution. Genome Biol 24:3
pubmed: 36624504
pmcid: 9830878
doi: 10.1186/s13059-022-02845-1
Wang RL, Stec A, Hey J, Lukens L, Doebley J (1999) The limits of selection during maize domestication. Nature 398:236–239
pubmed: 10094045
doi: 10.1038/18435
Wang L, Li J, Zhao J, He CY (2015) Evolutionary developmental genetics of fruit morphological variation within the Solanaceae. Front Plant Sci 6:248
pubmed: 25918515
pmcid: 4394660
Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859
pubmed: 1350515
doi: 10.1016/0092-8674(92)90295-N
Wilf P, Carvalho MR, Gandolfo MA, Cúneo NR (2017) Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355:71–75
pubmed: 28059765
doi: 10.1126/science.aag2737
Wingen LU, Münster T, Faigl W, Deleu W, Sommer H, Saedler H, Theißen G (2012) Molecular genetic basis of pod corn (Tunicate maize). Proc Natl Acad Sci USA 109:7115–7120
pubmed: 22517751
pmcid: 3344968
doi: 10.1073/pnas.1111670109
Wu J, Li P, Zhu D, Ma H, Li M, Lai Y, Peng Y, Li H, Li S, Wei J, Bian X, Rahman A, Wu S (2024) SlCRCa is a key D-class gene controlling ovule fate determination in tomato. Plant Biotechnol J 22:1966–1980
pubmed: 38561972
pmcid: 11182579
doi: 10.1111/pbi.14317
Xin H, Liu X, Chai S, Yang X, Li H, Wang B, Xu Y, Lin S, Zhong X, Liu B, Lu Z, Zhang Z (2024) Identification and functional characterization of conserved cis-regulatory elements responsible for early fruit development in cucurbit crops. Plant Cell 36:2272–2288
pubmed: 38421027
doi: 10.1093/plcell/koae064
Zeng H, Huang J, Ren J, Wang CK, Tang Z, Zhou H, Zhou Y, Shi H, Aditham A, Sui X, Chen H, Lo JA, Wang X (2023) Spatially resolved single-cell translatomics at molecular resolution. Science 380:eadd3067
pubmed: 37384709
pmcid: 11146668
doi: 10.1126/science.add3067
Zhang JS, Tian Y, Wang L, He CY (2010) Functional evolutionary developmental biology (evo-devo) of morphological novelties in plants. J Syst Evol 48:94–101
doi: 10.1111/j.1759-6831.2010.00066.x
Zhang JS, Khan MR, Tian Y, Li ZC, Simone R, He CY (2012) Divergences of MPF2-like MADS-domain proteins have an association with the evolution of the inflated calyx syndrome within Solanaceae. Planta 236:1247–1260
pubmed: 22711285
doi: 10.1007/s00425-012-1684-0
Zhang JS, Li ZC, Zhao J, Zhang SH, Quan H, Zhao M, He CY (2014) Deciphering the Physalis floridana Double-Layered Lantern1 mutant provides insights into functional divergence of the GLOBOSA duplicates within the Solanaceae. Plant Physiol 164:748–764
pubmed: 24390390
pmcid: 3912103
doi: 10.1104/pp.113.233072
Zhang T, Xu Z, Shang G, Wang J (2019) A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root. Mol Plant 12:648–660
pubmed: 31004836
doi: 10.1016/j.molp.2019.04.004
Zhao J, Tian Y, Zhang JS, Zhao M, Gong PC, 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
pubmed: 23792370
pmcid: 3723609
doi: 10.1105/tpc.113.111757
Zhou X, Stephens M (2012) Genome-wide efficient mixed-model analysis for association studies. Nat Genet 44:821–824
pubmed: 22706312
pmcid: 3386377
doi: 10.1038/ng.2310