Abstract
The size and shape of tomato (Solanum lycopersicum L.) fruit are determined by locule number. Gibberellin (GA) can increase locule number in tomato, but the underlying molecular mechanism is unclear. Therefore, in this study, multi-locule ‘MLK1’ tomato seedlings with two to three true leaves (pre-flower bud differentiation) were sprayed with GA1, GA3, GA4, GA7, PAC (paclobutrazol; an inhibitor of GA biosynthesis) and H2O, as a control. We found that GA4 resulted in was the most significant increase in tomato locule number among all bioactive GAs, while PAC decreased the locule number. We analyzed the change in locule number by RNA-seq, quantitative real-time PCR and ultra-performance liquid chromatography–tandem mass spectrometry. The categories ‘Phenylpropanoid biosynthesis’, ‘Plant hormone signal transduction’, and ‘Diterpenoid biosynthesis’ were considerably activated after spraying with GA4. Additionally, indole-3-acetic acid (IAA) content significantly increased and trans-Zeatin-riboside (tZ) content significantly reduced after exogenous GA4 application. We conclude that exogenous GA4 application changed the dynamic balance of hormones in the tomato shoot apex. Furthermore, 53 differentially expressed transcription factors were identified in tomato upon exogenous GA4 treatment during floral bud differentiation, including, YABBYs, TCP, NAC, and ARR (some directly regulate lateral organ development). Our results provide novel insights into how exogenous GA4 affects plant hormone homeostasis in the tomato shoot apex and the underlying mechanism of locule number regulation by GA4 in tomato.
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References
Bowman JL, Eshed Y (2000) Formation and maintenance of the shoot apical meristem. Trends Plant Sci 5:110–115
Buechel S, Leibfried A, To JPC, Zhao Z, Andersen SU, Kieber JJ, Lohmann JU (2010) Role of A-type ARABIDOPSIS RESPONSE REGULATORS in meristem maintenance and regeneration. Eur J Cell Biol 89:279–284. https://doi.org/10.1016/j.ejcb.2009.11.016
Cong B, Barrero L, Tanksley SD (2008a) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804
Cong B, Barrero LS, Tanksley SD (2008b) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 40:800–804
Eriksson S, Bohlenius H, Moritz T, Nilsson O (2006) GA4 Is the Active Gibberellin in the Regulation of LEAFY Transcription and Arabidopsis Floral Initiation. Plant Cell 18:2172–2181
Fleet CM, Sun T (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85
Galli M, Gallavotti A (2016) Expanding the regulatory network for meristem size in. Plants Trends Genet 32:372–383
Gimenez E et al (2010) Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS ONE 5:e14427. https://doi.org/10.1371/journal.pone.0014427
Giulini A, Wang J, Jackson D (2004) Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL. Nature 430 1:1031–1034
Gou J, Strauss SH, Tsai C, Fang K, Chen Y, Jiang X, Busov V (2010) Gibberellins regulate lateral root formation in populus through interactions with auxin and other hormones. Plant Cell 22:623–639
Guilfoyle TJ, Ulmasov T, Hagen G, THE ARF FAMILY OF TRANSCRIPTION FACTORS AND THEIR ROLE IN PLANT HORMONE-RESPONSIVE TRANSCRIPTION (1998) Cell Mol Life Sci 54:619–627
Hao Y et al (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68:302–313
Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444:11–25
Helliwell CA, Chandler PM, Poole AJ, Dennis ES, Peacock WJ (2001) The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proc Natl Acad Sci USA 98:2065–2070
Holt AL, Van Haperen JM, Groot EP, Laux T (2014) Signaling in shoot and flower meristems of Arabidopsis thaliana. Curr Opin Plant Biol 17:96–102
Ikeda A et al (2001) Slender Rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010
Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, Aharoni A (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. Plant J 60:1081–1095. https://doi.org/10.1111/j.1365-313X.2009.04064.x
Jain MK, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162
Jasinski S et al (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15:1560–1565
Liu S, Li TL (2012) Regulation effects of exogenous gibberellin acid (GA3) on the formation of tomato (Solanum lycoperscium) ovary locule and fasciated transcription. Afr J Biotechnol. https://doi.org/10.5897/ajb12.2244
Lee J, Baum SF, Alvarez JP, Patel A, Chitwood DH, Bowman JL (2005) Activation of CRABS CLAW in the nectaries and carpels of arabidopsis. Plant Cell 17:25–36
Lei Y et al (2018) Comparative analysis of alfalfa (Medicago sativa L.) leaf transcriptomes reveals genotype-specific salt tolerance mechanisms. BMC Plant Biol 18:35
Li C, Ng CKY, Fan L (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91
Li H et al (2017) Tomato transcription factor SlWUS plays an important role in tomato flower and locule development. Front Plant Sci 8:457
Li H et al (2017) Plant-specific histone deacetylases HDT1/2 regulate GIBBERELLIN 2-OXIDASE2 expression to control arabidopsis root meristem cell. Number Plant Cell 29:2183–2196. https://doi.org/10.1105/tpc.17.00366
Lippman Z, Tanksley SD (2001) Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom Genet 158:413–422
Lozano R, Gimenez E, Cara B, Capel J, Angosto T (2009) Genetic analysis of reproductive development in tomato. Int J Dev Biol 53:1635–1648
Mizoi J, Shinozaki K, Yamaguchishinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses ☆. Biochem Biophys Acta 1819:86–96
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475. https://doi.org/10.1016/j.cell.2006.05.050
Olszewski NE, Sun T, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:561–580
Pan IL, McQuinn R, Giovannoni JJ, Irish VF (2010a) Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 61:1795–1806. https://doi.org/10.1093/jxb/erq046
Pan X, Welti R, Wang X (2010b) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nat Protoc 5:986–992
Parapunova V et al (2014) Identification, cloning and characterization of the tomato TCP transcription factor family. BMC Plant Biol 14:157–157
Prabu G, Prasad DT (2012) Functional characterization of sugarcane MYB transcription factor gene promoter (PScMYBAS1) in response to abiotic stresses and hormones. Plant Cell Rep 31:661–669
Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518
Sakamoto T et al (2001) Expression of a gibberellin 2-oxidase gene around the shoot apex is related to phase transition in rice. Plant Physiol 125:1508–1516
Sawhney VK (1983) The role of temperature and its relationship with gibberellic acid in the development of floral organs of tomato (Lycopersicon esculentum). Botany 61:1258–1265
Serranomislata A, Bencivenga S, Bush M, Schiessl K, Boden SA, Sablowski R (2017) DELLA genes restrict inflorescence meristem function independently of plant height. Nat Plants 3:749–754
Shani E, Yanai O, Ori N (2006) The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 9:484–489
Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genomics 284:455–475
Shimada A et al (2008) Structural basis for gibberellin recognition by its receptor GID. Nature 456 1:520–523
Sun T, Kamiya Y (1997) Regulation and cellular localization of ent-kaurene synthesis. Physiol Plant 101:701–708
Sun T (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570
Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16:S181–S189
Xu C et al (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47:784–792
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
Yu H, Ito T, Zhao Y, Peng J, Kumar PP, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 101:7827–7832
Zhang L, Zhao G, Jia J, Liu XW, Kong X (2012) Molecular characterization of 60 isolated wheat MYB genes and analysis of their expression during abiotic stress. J Exp Bot 63:203–214
Zhang H et al (2018) Transcriptome characterization of moso bamboo (Phyllostachys edulis) seedlings in response to exogenous gibberellin applications. BMC Plant Biol 18:125
Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465:1089–1092
Zwack PJ, Rashotte AM (2015) Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot 66:4863–4871
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 31972397, U1708232), China Agriculture Research System (Grant No. CARS-25), and the Shenyang Scientific Research Project (18-013-0-36, RC180123).
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YL designed and carried out the experiments, analyzed the results, and wrote the manuscript. MS, HX, SM and BW provided scientific advice, and revised the manuscript. MQ and TL conceived the research area, provided scientific advice, and supervised the project.
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Table S1
The raw data of locule number investigation (XLSX 9.6 kb)
Table S2
The DEGs identified in GA4 vs. CK and PAC vs. CK (XLSX 89.1 kb)
Table S3
Gene Ontology analysis of DEGs in of GA4(100 µM), PAC (100 µM), and H2O treatments DEGs were annotated in three main categories: biological process, cellular component, and molecular function (DOCX 19.2 kb)
Table S4
Expression level and fold change of genes in RNA-seq (XLSX 10.8 kb)
Table S5
The raw data of qRT-PCR validation (XLSX 11.2 kb)
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Li, Y., Sun, M., Xiang, H. et al. Transcriptome analysis reveals regulatory effects of exogenous gibberellin on locule number in tomato. Plant Growth Regul 91, 407–417 (2020). https://doi.org/10.1007/s10725-020-00614-3
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DOI: https://doi.org/10.1007/s10725-020-00614-3