Expression profiling of Auxin and GA signaling genes during fruit set in Zanthoxylum armatum
DOI:
https://doi.org/10.15835/nbha53414536Keywords:
auxin, expression profiling, fruit set, gibberellin, Zanthoxylum armatumAbstract
Zanthoxylum armatum DC. is an important economic crop in Southwest China, but severe fruit drop and low fruit set rate reduce yields. Identification of key genes regulating fruit set in Z. armatum could provide new insights for addressing fruit abscission. In this study, we examined the morphological and anatomical characteristics of pistils and young fruits in two Z. armatum cultivars, ‘Jiuyeqing’ and ‘Prickleless’. Both cultivars exhibited unisexual flowers with apomictic traits and similar fruit morphology as well as anatomy. Transcriptome data were utilized to identify auxin and gibberellin biosynthetic and signaling genes. A total of 21 Aux/IAAs, 19 ARFs, 2 GA20oxs, 3 GA2OXs, GID1, and 6 DELLA genes were differentially expressed in male and female flowers, suggesting their candidate roles in regulating fruit set. Phylogenetic analysis revealed that Aux/IAA family members clustered into two clades with seven subfamilies, while ARFs were divided into four subclasses. ZaGA20oxs, ZaGA2oxs, ZaGID1, and ZaDELLAs showed high homology to their orthologs in tomato and cucumber. Quantitative real-time PCR (qRT-PCR) analysis showed that auxin-related ZaIAA8, ZaIAA11, ZaIAA20, ZaARF1, ZaARF5, and ZaARF10 exhibited similar expression trends during fruit set in both cultivars, whereas other genes (e.g., ZaIAA6, ZaIAA7, ZaARF9, ZaARF18) displayed divergent expression. Gibberellin-related ZaGA20ox2, ZaGA2OX2, ZaGA2OX4, ZaDELLA1, and ZaDELLA3 were significantly differentially expressed during pistil development and fruit initiation across cultivars. This study provides insights into the molecular mechanisms of phytohormone-mediated fruit development and offers a theoretical foundation for breeding high-yield varieties.
References
Bassa C, Mila I, Bouzayen M, Audran-Delalande C (2012). Phenotypes associated with down-regulation of Sl-IAA27 support functional diversity among Aux/IAA family members in tomato. Plant and Cell Physiology 53(9):1583-1595. https://doi.org/10.1093/pcp/pcs101
Chen S, Wang XJ, Zhang LY, Lin S, Liu D, Wang Q, ... Li Y (2016). Identification and characterization of tomato gibberellin 2-oxidases (GA2oxs) and effects of fruit-specific SlGA2ox1 overexpression on fruit and seed growth and development. Horticulture Research 3:16059. https://doi.org/10.1038/hortres.2016.59
De Jong M, Mariani C, Vriezen WH (2009). The role of auxin and gibberellin in tomato fruit set. Journal of Experimental Botany 60(5):1523-1532. https://doi.org/10.1093/jxb/erp094
Deng HP, Xu J, Chen F, Song QZ. (2008). Morphological and molecular identification on genetic diversity of Zanthoxylum armatum var. novem folius. Acta Botanica Boreali-Occidentalia Sinica 28(10):2103-2109.
Ding YF, Zeng WF, Wang XB, Wang Y, Niu L, Pan L, … Wang ZQ (2019). Over-expression of peach PpIAA19 in tomato alters plant growth, parthenocarpy, and fruit shape. Journal of Plant Growth Regulation 38:103-112. https://doi.org/10.1007/s00344-018-9813-z
Du LM, Bao CL, Hu TH,Zhu QM,Hu HJ, He QY, Mao WH (2016). SmARF8, a transcription factor involved in parthenocarpy in eggplant. Molecular Genetics and Genomics 291:93-105. https://doi.org/10.1007/s00438-015-1088-5
Enders TA, Strader LC (2015). Auxin activity: Past, present, and future. American Journal of Botany 102(2):180-196. https://doi.org/10.3732/ajb.1400285
Ezura K, Nomura Y, Ariizumi T (2023). Molecular, hormonal, and metabolic mechanisms of fruit set, the ovary-to-fruit transition, in horticultural crops. Journal of Experimental Botany 74(20):6254-6268. https://doi.org/10.1093/jxb/erad214
Fenn MA, Giovannoni JJ (2021). Phytohormones in fruit development and maturation. The Plant Journal 105(2):446-458. https://doi.org/10.1111/tpj.15112
Ferreira LG, de Alencar Dusi DM, Irsigler AST, Gomes ACMM, Mendes MA, Colombo L, de Campos Carneiro VT (2018). GID1 expression is associated with ovule development of sexual and apomictic plants. Plant Cell Reports 37:293-306. https://doi.org/10.1007/s00299-017-2230-0
Fuentes S, Ljung K, Sorefan K, Alvey E, Harberd NP, Stergaard L (2012). Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses. The Plant Cell 24(10):3982-3996. https://doi.org/10.1105/tpc.112.103192
Gallego‐Giraldo C, Hu JH, Urbez C, Gomez MD, Sun TP, Perez-Amador MA (2014). Role of the gibberellin receptors GID 1 during fruit‐set in Arabidopsis. The Plant Journal 79(6):1020-1032. https://doi.org/10.1111/tpj.12603
García-Hurtado N, Carrera E, Ruiz-Rivero O, López-Gresa MP, Hedden P, Gong F, García-Martínez JL (2012). The characterization of transgenic tomato overexpressing gibberellin 20-oxidase reveals induction of parthenocarpic fruit growth, higher yield, and alteration of the gibberellin biosynthetic pathway. Journal of Experimental Botany 63(16):5803-5813. https://doi.org/10.1093/jxb/ers229
Guan HL, Yang XL, Lin YX, Xie BX, Zhang XY, Ma CJ, … Hao YW (2024). The hormone regulatory mechanism underlying parthenocarpic fruit formation in tomato. Frontiers in Plant Science 15:1404980. https://doi.org/10.3389/fpls.2024.1404980
Heuvelink E, Körner O (2001). Parthenocarpic fruit growth reduces yield fluctuation and blossom-end rot in sweet pepper. Annals of Botany 88(1):69-74. https://doi.org/10.1006/anbo.2001.1427
Hu JH, Li X, Sun TP (2023). Four class A AUXIN RESPONSE FACTORs promote tomato fruit growth despite suppressing fruit set. Nature Plants 9(5):706-719. https://doi.org/10.1038/s41477-023-01396-y
Karlova R, Chapman N, David K, Angenent GC, Seymour GB, de Maagd RA (2014). Transcriptional control of fleshy fruit development and ripening. Journal of Experimental Botany 65(16):4527-4541. https://doi.org/10.1093/jxb/eru316
Kazan K, Manners JM (2009). Linking development to defense: auxin in plant-pathogen interactions. Trends in Plant Science 14(7):373-382. https://doi.org/10.1016/j.tplants.2009.04.005
Lakehal A, Chaabouni S, Cavel E, Hir RL, Ranjan A, Raneshan Z, … Bellini C (2019). A molecular framework for the control of adventitious rooting by TIR1/AFB2-Aux/IAA-dependent auxin signaling in Arabidopsis. Molecular Plant 12(11):1499-1514. https://doi.org/10.1016/j.molp.2019.09.001
Li BJ, Bao RX, Shi YN, Grierson D, Chen KS (2024). Auxin response factors: important keys for understanding regulatory mechanisms of fleshy fruit development and ripening. Horticulture Research 11(10):uhae209. https://doi.org/10.1093/hr/uhae209
Li C, Zheng LL, Wang XN, Hu ZB, Zheng Y, Chen QH, … Zhang YH (2019). Comprehensive expression analysis of Arabidopsis GA2-oxidase genes and their functional insights. Plant Science 285:1-13. https://doi.org/10.1016/j.plantsci.2019.04.023
Li WF, Zhou Q, Ma ZH, Zuo CW, Chu MY, Mao J, Chen BH (2024). Regulatory mechanism of GA3 application on grape (Vitis vinifera L.) berry size. Plant Physiology and Biochemistry 210:108543. https://doi.org/10.1016/j.plaphy.2024.108543
Liu B, Liu XW, Yang S, Chen CH, Xue SD, Cai YL, … Ren HZ (2016). Silencing of the gibberellin receptor homolog, CsGID1a, affects locule formation in cucumber (Cucumis sativus) fruit. New Phytologist 210(2):551-563. https://doi.org/10.1111/nph.13801
Liu ZH, Yu YC, Xiang FN (2011). Auxin response factors and plant growth and development. Heredity 33(12):1335-1346. https://doi.org/10.3724/sp.j.1005.2011.01335
Liu ZN, Miao LM, Huo RX, Song XY, Johnson C, Kong LJ, Sundaresan V, Yu XL (2018). ARF2-ARF4 and ARF5 are essential for female and male gametophyte development in Arabidopsis. Plant and Cell Physiology 59(1):179-189. https://doi.org/10.1093/pcp/pcx174
Luo J, Zhou JJ, Zhang JZ (2018). Aux/IAA gene family in plants: molecular structure, regulation, and function. International journal of molecular sciences 19(1):259. https://doi.org/10.3390/ijms19010259
Martínez-Bello L, Moritz T, López-Díaz I (2015). Silencing C19-GA 2-oxidases induces parthenocarpic development and inhibits lateral branching in tomato plants. Journal of Experimental Botany 66(19):5897-5910. https://doi.org/10.1093/jxb/erv300
Mazzucato A, Cellini F, Bouzayen M, Zouine M, Mila L, Minoia S, … Carriero F (2015). A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes. Molecular Breeding 35:1-15. https://doi.org/10.1007/s11032-015-0222-8
Plackett AR, Powers SJ, Fernandez-Garcia N, Urbanova T, Takebayashi Y, Seo M, … Hedden P (2012). Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1,-2, and-3 are the dominant paralogs. The Plant Cell 24(3):941-960. https://doi.org/10.1105/tpc.111.095109
Remington DL, Vision TJ, Guilfoyle TJ, Reed JW (2004). Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiology 135(3):1738-1752. https://doi.org/10.1104/pp.104.039669
Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012). Molecular regulation of seed and fruit set. Trends in Plant Science 17(11):656-665. https://doi.org/10.1016/j.tplants.2012.06.005
Serrani JC, Ruiz‐Rivero O, Fos M, García-Martínez JL (2008). Auxin‐induced fruit‐set in tomato is mediated in part by gibberellins. The Plant Journal 56(6):922-934. https://doi.org/10.1111/j.1365-313x.2008.03654.x
Sotelo-Silveira M, Marsch-Martínez N, de Folter S (2014). Unraveling the signal scenario of fruit set. Planta 239:1147-1158. https://doi.org/10.1007/s00425-014-2057-7
Sun TP (2011). The molecular mechanism and evolution of the GA–GID1–DELLA signaling module in plants. Current Biology 21(9):R338-R345. https://doi.org/10.1016/j.cub.2011.02.036
Sun XW, Duan ZX (1996). Progress in the studies on medicinal plants of the genus Zanthoxylum Linn. Acta Pharmaceutica Sinica 31(3):231-240
Tang N, Deng W, Hu GJ, Hu N, Li ZG (2015). Transcriptome profiling reveals the regulatory mechanism underlying pollination dependent and parthenocarpic fruit set mainly mediated by auxin and gibberellin. PLoS One 10(4):e0125355. https://doi.org/10.1371/journal.pone.0125355
Tantikanjana T, Nasrallah JB (2012). Non-cell-autonomous regulation of crucifer self-incompatibility by Auxin Response Factor ARF3. Proceedings of the National Academy of Sciences 109(47):19468-19473. https://doi.org/10.1073/pnas.1217343109
Wang HB, Wu T, Liu JL, Liu C, Zhu YF, Zhai H, … Xu LF (2020). PbGA20ox2 regulates fruit set and induces parthenocarpy by enhancing GA4 content. Frontiers in Plant Science 11:113. https://doi.org/10.3389/fpls.2020.00113
Wei H, Cheng YQ, Sun Y, Zhang XZ, He HL, Liu JF (2021) Genome-wide identification of the ARF gene family and ARF3 target genes regulating ovary initiation in hazel via ChIP sequencing. Frontiers in Plant Science 12:715820. https://doi.org/10.3389/fpls.2021.715820
Xu J, Zhu PY, Yao XF, Meng YJ, Lou L, Zhang M, … Xu JH(2024) Cucumber Auxin Response Factor CsARF10a Regulates Leaf Morphogenesis and Parthenocarpic Fruit Set in Tomato. Horticulturae 10(1):79. https://doi.org/10.3390/horticulturae10010079
Yang J, Tian L, Sun MX, Huang XY, Zhu J, Guan YH, Jia QS, Yang ZN (2013) AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiology 162(2):720-731. https://doi.org/10.1104/pp.113.214940
Yang WY, Wang L, Lv YK, Wang XB, Guo YT, Pu TS (2019). Comparative Analysis of Zanthoxylum Qualities Between ‘Rongchang Thornless’ and ‘Jiuyeqing’ Varieties. Journal of Sichuan Forestry Science and Technology 40(6):60-64.
Zhang X, Tang N, Liu XM, Ye JB, Zhang JY, Chen ZX, … Liao YL (2020). Comparative transcriptome analysis identified differentially expressed genes between male and female flowers of Zanthoxylum armatum var. novemfolius. Agronomy 10(2):283. https://doi.org/10.3390/agronomy10020283
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