The transcriptional control of LcIDL1–LcHSL2 complex by LcARF5 integrates auxin and ethylene signaling for litchi fruitlet abscission
Xingshuai Ma, Zidi He, Ye Yuan, Zhijian Liang, Hang Zhang, Vilde Olsson Lalun, Zhuoyi Liu, Yanqing Zhang, Zhiqiang Huang, Yulian Huang, Jianguo Li, Minglei Zhao
The transcriptional control of LcIDL1–LcHSL2 complex by LcARF5 integrates auxin and ethylene signaling for litchi fruitlet abscission
At the physiological level, the interplay between auxin and ethylene has long been recognized as crucial for the regulation of organ abscission in plants. However, the underlying molecular mechanisms remain unknown. Here, we identified transcription factors involved in indoleacetic acid (IAA) and ethylene (ET) signaling that directly regulate the expression of INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) and its receptor HAESA (HAE), which are key components initiating abscission. Specifically, litchi IDA-like 1 (LcIDL1) interacts with the receptor HAESA-like 2 (LcHSL2). Through in vitro and in vivo experiments, we determined that the auxin response factor LcARF5 directly binds and activates both LcIDL1 and LcHSL2. Furthermore, we found that the ETHYLENE INSENSITIVE 3-like transcription factor LcEIL3 directly binds and activates LcIDL1. The expression of IDA and HSL2 homologs was enhanced in LcARF5 and LcEIL3 transgenic Arabidopsis plants, but reduced in ein3 eil1 mutants. Consistently, the expressions of LcIDL1 and LcHSL2 were significantly decreased in LcARF5- and LcEIL3-silenced fruitlet abscission zones (FAZ), which correlated with a lower rate of fruitlet abscission. Depletion of auxin led to an increase in 1-aminocyclopropane-1-carboxylic acid (the precursor of ethylene) levels in the litchi FAZ, followed by abscission activation. Throughout this process, LcARF5 and LcEIL3 were induced in the FAZ. Collectively, our findings suggest that the molecular interactions between litchi AUXIN RESPONSE FACTOR 5 (LcARF5)–LcIDL1/LcHSL2 and LcEIL3–LcIDL1 signaling modules play a role in regulating fruitlet abscission in litchi and provide a long-sought mechanistic explanation for how the interplay between auxin and ethylene is translated into the molecular events that initiate abscission.
auxin / ethylene / fruit abscission / IDA–HAE/HSL2 / litchi
[1] |
Addicott, F.T. (1982). Abscission. University of California Press, Berkeley, Los Angeles, CA, London.
|
[2] |
Bleecker, A.B., and Patterson, S.E. (1997). Last exit: Senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9: 1169–1179.
|
[3] |
Butenko, M.A., Wildhagen, M., Albert, M., Jehle, A., Kalbacher, H., Aalen, R.B., and Felix, G. (2014). Tools and strategies to match peptide-ligand receptor pairs. Plant Cell 26: 1838–1847.
|
[4] |
Butenko, M.A., Patterson, S.E., Grini, P.E., Stenvik, G.E., Amundsen, S.S., Mandal, A., and Aalen, R.B. (2003). Inflorescencedeficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15: 2296–2307.
|
[5] |
Butenko, M.A., Stenvik, G.E., Alm, V., Saether, B., Patterson, S.E., and Aalen, R.B. (2006). Ethylene-dependent and -independent pathways controlling floral abscission are revealed to converge using promoter:: reporter gene constructs in the ida abscission mutant. J. Exp. Bot. 57: 3627–3637.
|
[6] |
Chang, K.N., Zhong, S., Weirauch, M.T., Hon, G., Pelizzola, M., Li, H., Huang, S.C., Schimitz, R.J., Urich, M.A., Kuo, D., et al. (2013). Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. eLife 2: e00675.
|
[7] |
Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., and Ecker, J.R. (1997). Activation of ethylene gas response pathway in Arabidopsis by the nuclear protein ethylene insensitive 3 and related proteins. Cell 89: 1133–1144.
|
[8] |
Cho, S.K., Larue, C.T., Chevalier, D., and Walker, J.C. (2008). Regulation of floral organ abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 105: 15629–15634.
|
[9] |
Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.
|
[10] |
Ecker, J.R. (1995). The ethylene signal transduction pathway in plants. Science 268: 667–675.
|
[11] |
Ellis, C.M., Nagpal, P., Young, J.C., Hagen, G., Guilfoyle, T.J., and Reed, J.W. (2005). AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132: 4563–4574.
|
[12] |
Estornell, L.H., Agustí, J., Merelo, P., Talón, M., and Tadeo, F.R. (2013). Elucidating mechanisms underlying organ abscission. Plant Sci. 199: 48–60.
|
[13] |
Estornell, L.H., Wildhagen, M., Pérez-Amador, M.A., Manuel, T., Tadeo, F.R., and Butenko, M.A. (2015). The IDA peptide controls abscission in Arabidopsis and citrus. Front. Plant Sci. 6: 1003.
|
[14] |
Feng, Y., Xu, P., Li, B., Li, P., Wen, X., An, F., Gong, Y., Xin, Y., Zhu, Z., Wang, Y., et al. (2017). Ethylene promotes root hair growth through coordinated EIN3/EIL1 and RHD6/RSL1 activity in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 114: 13834–13839.
|
[15] |
Galli, M., Khakhar, A., Lu, Z., Chen, Z., Sen, S., Joshi, T., Nemhauser, J.L., Schmitz, R.J., and Gallavotti, A. (2018). The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family. Nat. Commun. 9: 4526.
|
[16] |
Gao, Y., Liu, Y., Liang, Y., Lu, J., Jiang, C., Fei, Z., Jiang, C.Z., Ma, C., and Gao, J. (2019). Rosa hybrida RhERF1 and RhERF4 mediate ethylene- and auxin-regulated petal abscission by influencing pectin degradation. Plant J. 99: 1159–1171.
|
[17] |
Hagen, G., and Guilfoyle, T. (2002). Auxin-responsive gene expression: Genes, promoters and regulatory factors. Plant Mol. Biol. 49: 373–385.
|
[18] |
Hohmann, U., Santiago, J., Nicolet, J., Olsson, V., Spiga, F.M., Hothorn, L.A., Butenko, M.A., and Hothorn, M. (2018). Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors. Proc. Natl. Acad. Sci. U.S.A. 115: 3488–3493.
|
[19] |
Hu, G., Feng, J., Xiang, X., Wang, J., Salojärvi, J., Liu, C., Wu, Z., Zhang, J., Liang, X., Jiang, Z., et al. (2022). Two divergent haplotypes from a highly heterozygous lychee genome suggest independent domestication events for early and late-maturing cultivars. Nat. Genet. 54: 73–83.
|
[20] |
Jackson, A.C. (1992). Detection of rabies virus mRNA in mouse brain by using in situ hybridization with digoxigenin-labelled RNA probes. Mol. Cell. Probes. 6: 131–136.
|
[21] |
Jinn, T.L., Stone, J.M., Walker, J.C. (2000). HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev. 14: 108–117.
|
[22] |
La Rue, C.D. (1936). The effect of auxin on the abscission of petioles. Proc. Natl. Acad. Sci. U.S.A. 22: 254–259.
|
[23] |
Li, C.Q., Zhao, M.L., Ma, X.S., Wen, Z.X., Ying, P.Y., Peng, M.J., Ning, X.P., Xia, R., Wu, H., and Li, J.G. (2019). The HD-ZIP transcription factor LcHB2 regulates litchi fruit abscission through the activation of two cellulase genes. J. Exp. Bot. 70: 5189–5203.
|
[24] |
Li, R., Shi, C.L., Wang, X., Meng, Y., Cheng, L., Jiang, C.Z., Qi, M., Xu, T., and Li, T. (2021). Inflorescence abscission protein SlIDL6 promotes low light intensity-induced tomato flower abscission. Plant Physiol. 186: 1288–1301.
|
[25] |
Li, Y., Han, S., and Qi, Y. (2022). Advances in structure and function of auxin response factor in plants. J. Integr. Plant Biol. 65: 617–632.
|
[26] |
Liang, Y., Jiang, C., Liu, Y., Gao, Y., Lu, J., Aiwaili, P., Fei, Z., Jiang, C., Hong, B., Ma, C., et al. (2020). Auxin regulates sucrose transport to repress petal abscission in Rose (Rose Hybrida). Plant Cell 32: 3485–3499.
|
[27] |
Liljegren, S.J., Leslie, M.E., Darnielle, L., Lewis, M.W., Taylor, S.M., Luo, R., Geldner, N., Chory, J., Randazzo, P.A., Yanofsky, M.F., et al. (2009). Regulation of membrane trafficking and organ separation by the NEVERSHED ARF-GAP protein. Development 136: 1909–1918.
|
[28] |
Liu, C., Zhang, C., Fan, M., Ma, W., Chen, M., Cai, F., Liu, K., and Lin, F. (2018). GmIDL2a and GmIDL4a, encoding the inflorescence deficient in abscission-like protein, are involved in soybean cell wall degradation during lateral root emergence. Int. J. Mol. Sci. 19: 2262.
|
[29] |
Lombardi, L., Arrom, L., Mariotti, L., Battelli, R., Picciarelli, P., Kille, P., Stead, T., Munné-Bosch, S., and Rogers, H.J. (2015). Auxin involvement in tepal senescence and abscission in Lilium: A tale of two lilies. J. Exp. Bot. 66: 945–956.
|
[30] |
Ma, X.S., Li, C.Q., Huang, X.M., Wang, H.C., Wu, H., Zhao, M.L., and Li, J.G. (2019). Involvement of HD-ZIP I transcription factors LcHB2 and LcHB3 in fruitlet abscission by promoting transcription of genes related to the biosynthesis of ethylene and ABA in litchi. Tree Physiol. 39: 1600–1613.
|
[31] |
Ma, X.S., Yuan, Y., Wu, Q., Wang, J., Li, J.G., and Zhao, M.L. (2020). LcEIL2/3 are involved in fruitlet abscission via activating genes related to ethylene biosynthesis and cell wall remodeling in litchi. Plant J. 103: 1338–1350.
|
[32] |
Meir, S., Hunter, D.A., Chen, J.C., Halaly, V., and Reid, M.S. (2006). Molecular changes occurring during acquisition of abscission competence following auxin depletion in Mirabilis jalapa. Plant Physiol. 141: 1604–1616.
|
[33] |
Meir, S., Philosoph-Hadas, S., Salim, S., Segev, A., and Riov, J. (2022). Re-evaluation of ethylene role in Arabidopsis cauline leaf abscission induced by water stress and rewatering. Plant Direct 6: e444.
|
[34] |
Meir, S., Philosoph-Hadas, S., Sundaresan, S., Selvaraj, K.S., Burd, S., Ophir, R., Kochanek, B., Reid, M.S., Jiang, C.Z., and Lers, A. (2010). Microarray analysis of the abscission-related transcriptome in the tomato flower abscission zone in response to auxin depletion. Plant Signal. Behav. 154: 1929–1956.
|
[35] |
Mirdita, M., Schutze, K., Moriwaki, Y., Heo, L., Ovchinnikov, S., and Steinegger, M. (2022). ColaFold: Making protein folding accessible to all. Nat. Methods 19: 679–682.
|
[36] |
Okushima, Y., Overvoode, P.J., Arima, K., Alonso, J.M., Chan, A., Chang, C., Ecker, J.R., Hughes, B., Lui, A., Nguyen, D., et al. (2005). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell 17: 444–463.
|
[37] |
Olsson, V., and Butenko, M.A. (2018). Abscission in plants. Curr. Biol. 28: R329–R341.
|
[38] |
Patterson, S.E. (2001). Cutting loose abscission and dehiscence in Arabidopsis. Plant Physiol. 126: 494–500.
|
[39] |
Roberts, J.A., and Gonzalez-Carranza, Z.H. (2007). Plant cell separation and adhesion. Annu. Rev. Plant Biol. 25: 479–480.
|
[40] |
Roberts, J.A., Elliott, K.A., and Gonzalez-Carranza, Z.H. (2002). Abscission, dehiscence, and other cell separation processes. Annu. Rev. Plant Biol. 53: 131–158.
|
[41] |
Santiago, J., Brandt, B., Wildhagen, M., Hohmann, U., Hothorn, L.A., Butenko, M.A., and Hothorn, M. (2016). Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5: e15075.
|
[42] |
Sexton, R. (1982). Cell biology of abscission. Annu. Rev. Physiol. 33: 133–162.
|
[43] |
Shen, X., Li, Y., Pan, Y., and Zhong, S. (2016). Activation of HLS1 by mechanical stress via ethylene-stabilized EIN3 is crucial for seedling soil emergence. Front. Plant Sci. 7: 1571.
|
[44] |
Shi, C.L., Alling, R.M., Hammerstad, M., and Aalen, R.B. (2019). Control of organ abscission and other cell separation processes by evolutionary conserved peptide signaling. Plants 8: 225.
|
[45] |
Shin, J., Mila, I., Liu, M., Rodrigues, M.A., Vernoux, T., Pirrello, J., and Bouzayen, M. (2019). The RIN-regulated small auxin-up RNA SAUR69 is involved in the unripe-to-ripe phase transition of tomato fruit via enhancement of the sensitivity to ethylene. New Phytol. 222: 820–836.
|
[46] |
Singh, P., Maurya, S.K., Singh, D., and Sane, A.P. (2023). The rose INFLORESCENCE DEFICIENT IN ABSCISSION-LIKE genes, RbIDL1 and RbIDL4, regulate abscission in an ethylene-responsive manner. Plant Cell Rep. 42: 1147–1161.
|
[47] |
Solano, R., Stepanova, A., Chao, Q., and Ecker, J.R. (1998). Nuclear events in ethylene signaling: A transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12: 3703–3714.
|
[48] |
Stenvik, G.E., Tandstad, N.M., Guo, Y.F., Shi, C.L., Kristiansen, W., Holmgren, A., Clark, S.E., Aalen, R.B., and Butenko, M.A. (2008). The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission on Arabidopsis through the Receptor-Like Kinases HAESA and HAESA-LIKE2. Plant Cell 20: 1805–1817.
|
[49] |
Stø, I.M., Orr, R.J., Fooyontphanich, K., Jin, X., Knutsen, J.M., Fischer, U., Tranbarger, T.J., Nordal, I., and Aalen, R.B. (2015). Conservation of the abscission signaling peptide IDA during Angiosperm evolution: Withstanding genome duplications and gain and loss of the receptors HAE/HSL2. Front. Plant Sci. 6: 931.
|
[50] |
Sundaresan, S., Philosoph-Hadas, S., Riov, J., Belausov, E., Kochanek, B., Tucker, M.L., and Meir, S. (2015). Abscission of flowers and floral organs is closely associated with alkalization of the cytosol in abscission zone cells. J. Exp. Bot. 66: 1355–1368.
|
[51] |
Taylor, J.E., and Whitelaw, C.A. (2001). Signals in abscission. New Phytol. 151: 323–340.
|
[52] |
Tian, Y., Chen, Z., Jiang, Z., Huang, X., Zhang, L., Zhang, Z., and Sun, P. (2022). Effects of plant growth regulators on flower abscission and growth of tea plant Camellia sinensis (L.) O. Kuntze. J. Plant Growth Regul. 41: 1161–1173.
|
[53] |
Tieman, D.M., Ciardi, J.A., Taylor, M.G., and Klee, H.J. (2001). Members of the tomato SlEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J. 26: 47–58.
|
[54] |
Tucker, M.L., and Yang, R. (2012). IDA-like gene expression in soybean and tomato leaf abscission and requirement for a diffusible stelar abscission signal. AoB Plants 2012: 35.
|
[55] |
Wang, F., Zheng, Z., Yuan, Y., Li, J., and Zhao, M.L. (2019). Identification and characterization of HAESA-like genes involved in the fruitlet abscission in litchi. Int. J. Mol. Sci. 20: 5945.
|
[56] |
Whitelaw, C.A., Nicholas, N.L., Chen, L., Zhou, D., Mattoo, A.K., and Tucker, M.L. (2002). Delayed abscission and shorter internodes correlate with a reduction in the ethylene receptor LeETR1 transcript in transgenic tomato. Plant Physiol. 128: 978–987.
|
[57] |
Wilmowicz, E., Kucko, A., Pokora, W., Kapusta, M., Jasieniecka-Gazarkiewica, K., Tranbarger, T.J., Wolska, M., and Panek, K. (2021). EPIP-evoked modifications of redox, lipid, and pectin homeostasis in the abscission zone of Lupine flowers. Int. J. Mol. Sci. 22: 3001.
|
[58] |
Wilmowicz, E., Kućko, A., Ostrowski, M., and Panek, K. (2018). INFLORESCENCE DEFICIENT IN ABSCISSION-like is an abscission-associated and phytohormone-regulated gene in flower separation ofLupinus luteus. Plant Growth Regul. 85: 91–100.
|
[59] |
Yamasaki, K., Kigawa, T., Inoue, M., Yamasaki, T., Yabuki, T., Aoki, M., Seki, E., Matsuda, T., Tomo, Y., Terada, T., et al. (2005). Solution structure of the major DNA-binding domain of Arabidopsis thaliana ethylene-insensitive3-like3. J. Mol. Biol. 348: 253–264.
|
[60] |
Yang, M., Hu, X., Ouyang, X., Muhammad, S., Ma, X., and Yuan, D. (2021). Molecular cloning and characterization of three CoIDA genes in Camellia oleifera. Braz. J. Bot. 41: 391–400.
|
[61] |
Yang, Q., Meng, D., Gu, Z., Li, W., Chen, Q., Li, Y., Yuan, H., Yu, J., Liu, C., and Li, T. (2018). Apple S-RNase interacts with an actin-binding protein, MdMVG, to reduce pollen tube growth by inhibiting its actin-severing activity at the early stage of self-pollination induction. Plant J. 95: 41–56.
|
[62] |
Ying, P., Li, C., Liu, X., Xia, R., Zhao, M., and Li, J. (2016). Identification and molecular characterization of an IDA-like gene from litchi, LcIDL1, whose ectopic expression promotes floral organ abscission in Arabidopsis. Sci. Rep. 6: 37135.
|
[63] |
Zhang, Y., Zeng, Z., Chen, C., Li, C., Xia, R., and Li, J. (2019). Genome-wide characterization of the auxin response factor (ARF) gene family of litchi (Litchi chinensis Sonn.): Phylogenetic analysis, miRNA regulation and expression changes during fruit abscission. Peer J. 7: 6677.
|
[64] |
Zhao, H., Yin, C.C., Ma, B., Chen, S.Y., and Zhang, J.S. (2021). Ethylene signaling in rice and Arabidopsis: New regulators and mechanism. J. Integr. Plant Biol. 63: 102–125.
|
[65] |
Zhao, M., and Li, J. (2020). Molecular events involved in fruitlet abscission in litchi. Plants 9: 151.
|
[66] |
Zhong, H.Y., Chen, J.W., Li, C.Q., Chen, L., Wu, J.Y., Chen, J.Y., Lu, W.J., and Li, J.G. (2011). Selection of reliable reference genes for expression studies by reverse transcription quantitative real-time PCR in litchi under different experimental conditions. Plant Cell Rep. 30: 641–653.
|
/
〈 | 〉 |