Cytokinin-induced parthenocarpy of San Pedro type fig (Ficus carica L.) main crop: explained by phytohormone assay and transcriptomic network comparison
CPPU-induced San Pedro type fig main crop parthenocarpy exhibited constantly increasing IAA content and more significantly enriched KEGG pathways in the receptacle than in female flowers.
N-(2-chloro-4-pyridyl)-N-phenylurea (CPPU) was applied to San Pedro fig (Ficus carica L.) main crop to induce parthenocarpy; the optimal effect was obtained with 25 mg L−1 application to syconia when female flowers were at anthesis. To elucidate the key expression changes in parthenocarpy conversion, significant changes in phytohormone level and transcriptome of fig female flowers and receptacles were monitored. HPLC–MS revealed increased IAA content in female flowers and receptacle 2, 4 and 10 days after treatment (DAT), decreased zeatin level in the receptacle 2, 4 and 10 DAT, decreased GA3 content 2 and 4 DAT, and increased GA3 content 10 DAT. ABA level increased 2 and 4 DAT, and decreased 10 DAT. CPPU-treated syconia released more ethylene than the control except 2 DAT. RNA-Seq and bioinformatics analysis revealed notably more differentially expressed KEGG pathways in the receptacle than in female flowers. In the phytohormone gene network, GA-biosynthesis genes GA20ox and GA3ox were upregulated, along with GA signal-transduction genes GID1 and GID2, and IAA-signaling genes AUX/IAA and GH3. ABA-biosynthesis gene NCED and signaling genes PP2C and ABF were downregulated 10 DAT. One ACO gene showed consistent upregulation in both female flowers and receptacle after CPPU treatment, and more than a dozen of ERFs demonstrated opposing changes in expression. Our results revealed early-stage spatiotemporal phytohormone and transcriptomic responses in CPPU-induced San Pedro fig main crop parthenocarpy, which could be valuable for further understanding the nature of the parthenocarpy of different fig types.
KeywordsCytokinin treatment Fig (Ficus carica L.) Parthenocarpy Phytohormone San Pedro fig Transcriptome
This work was supported by National Natural Science Foundation of China project NSFC .
HM and PC designed the experiments. PC and LC conducted the experiments and analyzed the results. SD carried out the CPPU treatment again and performed the ethylene assay in 2018. PC, SD, LC, HM, SC and MF prepared the manuscript. All authors have read and approved the manuscript for publication.
- Ainalidou A, Tanou G, Belghazi M, Samiotaki M, Diamantidis G, Molassiotis A, Karamanoli K (2016) Integrated analysis of metabolites and proteins reveal aspects of the tissue-specific function of synthetic cytokinin in kiwifruit development and ripening. J Proteom 143:318–333. https://doi.org/10.1016/j.jprot.2016.02.013 Google Scholar
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc 57(1):289–300Google Scholar
- Chai L, Wang Z, Chai P, Chen S, Ma H (2017) Transcriptome analysis of San Pedro-type fig (Ficus carica L.) parthenocarpic breba and non-parthenocarpic main crop reveals divergent phytohormone-related gene expression. Tree Genet Genomes 13(4):83. https://doi.org/10.1007/s11295-017-1166-4 Google Scholar
- Flaishman MA, Rodov V, Stover E (2008) The fig: botany, horticulture, and breeding. Hortic Rev 34:113–196Google Scholar
- Fu FQ, Mao WH, Shi K, Zhou YH, Yu JQ (2010) Spatio-temporal changes in cell division, endoreduplication and expression of cell cycle-related genes in pollinated and plant growth substances-treated ovaries of cucumber. Plant Biol (Stuttg) 12(1):98–107. https://doi.org/10.1111/j.1438-8677.2009.00203.x Google Scholar
- Hayata Y, Niimi Y, Iwasaki N (1995) Synthetic cytokinin-1-(2= chloro= 4= pyridyl)-3-phenylurea (CPPU)-promotes fruit set and induces parthenocarpy in watermelon. J Am Soc Hortic Sci 120(6):997–1000Google Scholar
- Hossain MA, Lee Y, Cho J, Ahn C, Lee S, Jeon J, Kang H, Lee C, An G, Park PB (2010) The bZIP transcription factor osABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol 72(4–5):557–566. https://doi.org/10.1007/s11103-009-9592-9 Google Scholar
- Jones B, Gunnerås SA, Petersson SV, Tarkowski P, Graham N, May S, Dolezal K, Sandberg G, Ljung K (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22(9):2956–2969. https://doi.org/10.1105/tpc.110.074856 Google Scholar
- Koiwai M, Okuyama F, Tanaka KI, Yamazaki A, Honma H, Ikeda K, Taira S (2012) Induction of parthenocarpy by GA and CPPU treatments aimed for seedless berry production in female vines of Japanese wild grape, Vitis coignetiae Pulliat. Hortic Res 11:87–95Google Scholar
- Kondo S, Kawai M (1998) Relationship between free and conjugated ABA levels in seeded and gibberellin-treated seedless, maturing ‘Pione’ grape berries. J Am Soc Hortic Sci 123(5):750–754Google Scholar
- Li Y, Yu JQ, Ye QJ, Zhu ZJ, Guo ZJ (2003) Expression of CycD3 is transiently increased by pollination and N-(2-chloro-4-pyridyl)-N′-phenylurea in ovaries of Lagenaria leucantha. J Exp Bot 54(385):1245–1251Google Scholar
- Li J, Wu Z, Cui L, Zhang T, Guo Q, Xu J, Jia L, Luo Q, Huang S, Li Z, Chen J (2014) Transcriptome comparison of global distinctive features between pollination and parthenocarpic fruit set reveals transcriptional phytohormone cross-talk in cucumber (Cucumis sativus L.). Plant Cell Physiol 55(7):1325–1342. https://doi.org/10.1093/pcp/pcu051 Google Scholar
- Liu M, Gomes BL, Mila I, Purgatto E, Peres LE, Frasse P, Maza E, Zouine M, Roustan JP, Bouzayen M, Pirrello J (2016) Comprehensive profiling of ethylene response factors expression identifies ripening-associated ERF genes and their link to key regulators of fruit ripening in tomato (Solanum lycopersicum). Plant Physiol 170(3):1732–1744. https://doi.org/10.1104/pp.15.01859 Google Scholar
- Nishitani C, Yamaguchi-Nakamura A, Hosaka F, Terakami S, Shimizu T, Yano K, Itai A, Saito T, Yamamoto T (2012) Parthenocarpic genetic resources and gene expression related to parthenocarpy among four species in pear (Pyrus, spp.). Sci Hortic 136(2):101–109. https://doi.org/10.1016/j.scienta.2011.12.029 Google Scholar
- Serrani JC, Carrera E, Ruiz-Rivero O, Gallego-Giraldo L, Peres LE, García-Martínez JL (2010) Inhibition of auxin transport from the ovary or from the apical shoot induces parthenocarpic fruit-set in tomato mediated by gibberellins. Plant Physiol 153(2):851–862. https://doi.org/10.1104/pp.110.155424 Google Scholar
- Shinozaki Y, Hao S, Kojima M, Sakakibara H, Ozeki-Iida Y, Zheng Y, Fei Z, Zhong S, Giovannoni JJ, Rose JK, Okabe Y, Heta Y, Ezura H, Ariizumi T (2015) Ethylene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism. Plant J 83(2):237–251. https://doi.org/10.1111/tpj.12882 Google Scholar
- Vivian-Smith A, Koltunow AM (1999) Genetic analysis of growth regulator-induced parthenocarpy in arabidopsis. Plant Physiol 121:437–451Google Scholar
- Wang H, Schauer N, Usadel B, Frasse P, Zouine M, Hernould M, Latché A, Pech JC, Fernie AR, Bouzayen M (2009) Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 21(21):1428–1452. https://doi.org/10.1105/tpc.108.060830 Google Scholar
- Weiblen GD (2002) How to be a fig wasp. Ann Rev Entomol 47(1):299–330. https://doi.org/10.1146/annurev.ento.47.091201.145213 Google Scholar
- Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15(11):2532–2550. https://doi.org/10.1105/tpc.014928 Google Scholar
- Ye X, Fu M, Liu Y, An D, Zheng X, Tan B, Li J, Cheng J, Wang W, Feng J (2018) Expression of grape ACS1 in tomato decreases ethylene and alters the balance between auxin and ethylene during shoot and root formation. J Plant Physiol 226:154–162. https://doi.org/10.1016/j.jplph.2018.04.015 Google Scholar