Abstract
Fruit shape is one of the important traits for quality evaluation, classification, and market grading of horticultural crops. In order to explore the genes regulating pear fruit shape formation, pear varieties ‘Huangguan’ and ‘Korla Fragrant Pear’ with significant differences in fruit shape were selected as experimental materials. Through morphological observation, measurement of fruit longitudinal diameter and fruit transverse diameter, and fruit shape index analysis of the pear fruit growth and development period, the formation of pear fruit shape during the young fruit period was preliminarily determined. By analyzing the transcriptome data of ‘Huangguan’ and ‘Korla Fragrant Pear’ at the young fruit stage, 8993 differentially expressed genes were obtained, and the majority of the genes were annotated to the plant hormone signaling pathway, among which gibberellin-related genes accounted for 13.4%. Spraying GA3 at the full-bloom stage can significantly prolong the shape of oriental pear. The results of qRT-PCR showed that the expression level of the gibberellin metabolic pathway gene PbGA2ox11 in ‘Huangguan’ was significantly higher than that in ‘Korla Fragrant Pear’. GA3 treatment inhibited the expression of this gene in ‘Korla Fragrant Pear’, while PP333 promoted the expression. It was speculated that PbGA2ox11 was most likely to regulate the shape of pear fruit by regulating gibberellin metabolism. This study provides a new method for studying fruit shape via the analysis of the gibberellin synthesis metabolic pathway, new resources for the rational use of plant growth regulators, and theoretical and technical support for cultivating excellent fruit shape.
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Data availability
All data used and analyzed during this research are included in this article and its additional files. The RNA-seq reads, including ovary, petal, flower, leaves, sepal, bud, stem, and seven pear fruit development stages, were obtained from NCBI (PRJNA309745) (Cao et al. 2019a). The transcriptome data of ‘Huangguan ’were provided by the pear research group of College of Horticulture, Shanxi Agricultural University.
References
Bain JM (1961) Some morphological, anatomical, and physiological changes in the pear fruit (Pyrus Communis var. Williams Bon Chrétien) during development and following harvest. Aust J bot 9(2):239–257. https://doi.org/10.1071/BT9610099
Bidadi H, Yamaguchi S, Asahina M et al (2010) effects of shoot-applied gibberellin/gibberellin-biosynthesis inhibitors on root growth and expression of gibberellin biosynthesis genes in Arabidopsis thaliana. Plant Root 4:4–11. https://doi.org/10.3117/plantroot.4.4
Biemelt S, Tschiersch Henning S (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135(1):254–265. https://doi.org/10.1104/pp.103.036988
Bleecker AB, Schuette JL, Kende H (1986) Anatomical analysis of growth and developmental patterns in the internode of deepwater rice. Planta 169(4):490–497. https://doi.org/10.1007/BF00392097
Cao YF (2006) Description and data standard of pear germplasm resources. China Agricultural Publishing House, Beijing
Cao YP, Li XX, Jiang L (2019) Integrative analysis of the core fruit lignification toolbox in pear reveals targets for fruit quality bioengineering. Biomolecules 9(9):504. https://doi.org/10.3390/biom9090504
Chen S, Wang XJ, Tan GF et al (2020) Gibberellin and the plant growth retardant paclobutrazol altered fruit shape and ripening in tomato. Protoplasma 257(3):853–861. https://doi.org/10.1007/s00709-019-01471-2
Christodoulou A, Pool R, Weaver R (1966) Prebloom thinning of Thompson seedless grapes is feasible when followed by bloom spraying with gibberellin. Calif Agric 20(11):8–10
Cruz-Castillo JG, Woolley DJ, Lawes GS (2002) Kiwifruit size and CPPU response are influenced by the time of anthesis. Sci Hortic 95(1–2):23–30. https://doi.org/10.1016/S0304-4238(01)00384-3
Davies P, Davies P, Krikorian AD (1996) Plant hormones: physiology, biochemistry and molecular biology. Sci Hort 66(3):267–270. https://doi.org/10.3389/fphys.2021.644907
Du Y (2013) Study on the formation mechanism and regulation of fruit shape of Fuji apple in akesu, Xinjiang Agricultural University. https://doi.org/10.1016/j.plaphy.2020.06.044
Effie MG, Hedden P et al (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60(7):1979–1989. https://doi.org/10.1093/jxb/erp040
Gao HJ, Li P, Dong T (2016) Advances in the study off actors influencing fruit shape. J Trop Biology 2:279–284. https://doi.org/10.15886/j.cnki.rdswxb.2016.02.024
Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99(6):978–987. https://doi.org/10.1007/s001220051405
Guo J, Zhou YJ, Hillwig ML et al (2013) CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts. Proc Natl Acad Sci USA 110(29):12108–12113. https://doi.org/10.1073/pnas.1218061110
Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5(12):523–530. https://doi.org/10.1016/S1360-1385(00)01790-8
Huang YP, Xiong J, Xiong M et al (2019) Comparative analysis of seven famous pears quality. Beverage Ind 05:1–4
Jiang ZA, Peng JY, Sun JS (2014) Isolation and expression of MdKS and MdKOA1 Gene in Apple. J Plant Genet Resour 15(2):362–368. https://doi.org/10.13430/j.cnki.jpgr.2014.02.020
Ke ZJ (2015) Variation of major storage materials and expressionAnalysis of gibberellins metabolic enzyme genesduring seed germination in foxtail millet. Shanxi Agricultural University
Kende H, Zeevaart JAD (1997) The five classical plant hormones. Plant Cell 9(7):1197–1210. https://doi.org/10.1105/tpc.9.7.1197
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360. https://doi.org/10.1038/nmeth.3317
Lange T, Hedden P, Graebe JE (1994) Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proc Natl Acad Sci USA 91(18):8552–8556. https://doi.org/10.1073/pnas.91.18.8552
Li HX, Niu JJ, Wang XN et al (2007) Screening test of pollinated varieties of ‘Huangguan’ pear. Chin Fruit Trees 6:18–20. https://doi.org/10.16626/j.cnki.issn1000-8047.2007.06.011
Liang B, Zhang JQ, Ren F et al (2020) Cloning and expression analysis of ent-kaurene oxidase gene CCKO in carya cathayensis. Sci Silvae Sinicae 56(10):70–82
Liao X, Li M, Liu B et al (2018) Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. Proc Natl Acad Sci 115(49):E11542–E11550. https://doi.org/10.1073/pnas.1812575115
Liu Y, Wang YB, Li JH et al (2019) Responses of intracellular ca2+ and its sensors to venturia nashicola infection in pear (Pyrus Bretschneideri) differing resistance. Sci Hortic 243(3):552–558. https://doi.org/10.1016/j.scienta.2018.09.010
Livak KJ, Schmittgen TD (2013) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80. https://doi.org/10.1105/tpc.010476
Peng DL, Chen XG, Yin YP et al (2014) Lodging resistance of winter wheat (Triticum aestivum L.): lignin accumulation and its related enzymes activities due to the application of paclobutrazol or gibberellin acid. Field Crop Res 157(15):1–7. https://doi.org/10.1016/j.fcr.2013.11.015
Pertea M, Pertea GM, Antonescu CM et al (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–295. https://doi.org/10.1038/nbt.3122
Qiao J, Liu FZ, ChenYH et al (2011) Research progress on lnheritance of fruit shape in horticultural crops. Acta Hortic Sinica 7:1385–1396. https://doi.org/10.16420/j.issn.0513-353x.2011.07.024
Rai N, Nath A, Yadav DS et al (2003) Effect of different concentration of paclobutrazol PP333 on growth, flowering and quality of bottle gourd. Agric Sci Digest 23(1):44–46
Sakamoto T, Morinaka Y, Ishiyama K et al (2003) Genetic manipulation of gibberellin metabolism in transgenic rice. Nat Biotechnol 21(8):909–913. https://doi.org/10.1038/nbt847
Schomburg FM, Bizzell CM, Lee DJ et al (2003) Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell 15(1):151–163. https://doi.org/10.1105/tpc.005975
Seymour GB, Granell A (2014) Fruit development and ripening. J Exp Bot. https://doi.org/10.1146/annurev-arplant-050312-120057
Shinjiro Y (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol. https://doi.org/10.1146/annurev.arplant.59.032607.092804
Sho Miyazaki T, Katsumata MN, Kawaide H (2011) The CYP701B1 of Physcomitrella patens is an ent-kaurene oxidase that resists inhibition by uniconazole-P. FEBS Lett 585(12):1879–1883. https://doi.org/10.1016/j.febslet.2011.04.057
Tan B, Wang T, Hao PB et al (2019) Effects of GA3 and PBZ on shoot growth and expression of GA-related genes in peach. J North China Agric 02:25–34
Tang YH, Zhnag DL, Gu JJ (2013) Dwarfing effect of different growth retardants on potted roses. Jiangsu Agric Sci 3:138–140
Toshiya Y, Shingo T (2016) Genomics of pear and other Rosaceae fruit trees. Breed Sci 66:148–159. https://doi.org/10.1270/jsbbs.66.148
Williams MW, Stahly EA (1969) Effect of cytokinins and gibberellins on shape of ‘delicious’ apple fruits. J Am Soc Hortic Sci 94(1):17–18. https://doi.org/10.21273/JASHS.94.1.17
Yang YH, Zhang YD, Zhu Z et al (2010) Effects of gibberellic acid 3 and abscisic acid on growth, physiological characteristics and gene expression of GA20ox2 and GA3ox2 in different rice cultivars Chinese. J Rice Sci 04:433–437
Zhang Y, Huang GD, Rong T et al (2023) Cloning, subcellular localization and expression analysis of GA3ox gibberellin oxidase gene in Mango. Mol Plant Breed 21(4):1111–1116. https://doi.org/10.13271/j.mpb.021.001111
Zhang H, Li M, He DL et al (2020) Mutations on ent-kaurene oxidase 1 encoding gene attenuate its enzyme activity of catalyzing the reaction from ent-kaurene to ent-kaurenoic acid and lead to delayed germination in rice. PLoS Genet 16(1):e1008562. https://doi.org/10.1371/journal.pgen.1008562
Zhang DH, Xu QX, Li LM et al (1999) Study on fruit shape variation of Korla fragrant pear. Xinjiang Agric Sci 06:261–263
Zhao L, Qi D, Zeng J et al (2012) An improved CTAB-ammonium acetate method for total RNA isolation from cotton. Phytochem Anal 23:647–650. https://doi.org/10.1002/pca.2368
Acknowledgements
The authors thank all contributors to this research for their help. This research was financially supported by the Central Leading Local Science and Technology Development Fund Project (Grant No. YDZJSX2022A042), and the Biological Breeding Project of Shanxi Agricultural University (Grant No. YZGC109), and the Scientific and Postgraduate Innovation Project of Shanxi Province (Grant No. 2021Y322).
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ZX contributed by methodology, data curation, writing the manuscript. RY contributed by checking the experimental data. YW contributed to the manuscript editing. YM, YL and ZL contributed by methodology. YS, XF and LL contributed by conceptualization, supervision, manuscript editing. All authors have read and approved the final manuscript.
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Xue, Z., Yang, R., Wang, Y. et al. Candidate gene mining of GA-mediated regulation of pear fruit shape. Hortic. Environ. Biotechnol. (2024). https://doi.org/10.1007/s13580-023-00574-3
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DOI: https://doi.org/10.1007/s13580-023-00574-3