The RING-H2 gene LdXERICO plays a negative role in dormancy release regulated by low temperature in Lilium davidii var. unicolor

Xinyue Fan , Xiaoman Zou , Linlan Fu , Yue Yang , Min Li , Chunxia Wang , Hongmei Sun

Horticulture Research ›› 2023, Vol. 10 ›› Issue (4) : 030

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (4) :030 DOI: 10.1093/hr/uhad030
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The RING-H2 gene LdXERICO plays a negative role in dormancy release regulated by low temperature in Lilium davidii var. unicolor
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Abstract

Dormancy regulation is the basis of the sustainable development of the lily industry. Therefore, basic research on lily dormancy is crucial for innovation in lily cultivation and breeding. Previous studies revealed that dormancy release largely depends on abscisic acid (ABA) degradation. However, the key genes and potential regulatory network remain unclear. We used exogenous ABA and ABA inhibitors to elucidate the effect of ABA on lily dormancy. Based on the results of weighted gene coexpression network analysis (WGCNA), the hub gene LdXERICO was identified in modules highly related to endogenous ABA, and a large number of coexpressed genes were identified. LdXERICO was induced by exogenous ABA and expressed at higher levels in tissues with vigorous physiological activity. Silencing LdXERICO increased the low-temperature sensitivity of bulblets and accelerated bulblet sprouting. LdXERICO rescued the ABA insensitivity of xerico mutants during seed germination in Arabidopsis, suggesting that it promotes seed dormancy and supporting overexpression studies on lily bulblets. The significant increase in ABA levels in transgenic Arabidopsis expressing LdXERICO indicated that LdXERICO played a role by promoting ABA synthesis. We generated three transgenic lines by overexpressing LdICE1 in Arabidopsis thaliana and showed that, in contrast to LdXERICO, LdICE1 positively regulated dormancy release. Finally, qRT–PCR confirmed that LdXERICO was epistatic to LdICE1 for dormancy release. We propose that LdXERICO, an essential gene in dormancy regulation through the ABA-related pathway, has a complex regulatory network involving temperature signals. This study provides a theoretical basis for further exploring the mechanism of bulb dormancy release.

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Xinyue Fan, Xiaoman Zou, Linlan Fu, Yue Yang, Min Li, Chunxia Wang, Hongmei Sun. The RING-H2 gene LdXERICO plays a negative role in dormancy release regulated by low temperature in Lilium davidii var. unicolor. Horticulture Research, 2023, 10 (4) : 030 DOI:10.1093/hr/uhad030

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Acknowledgements

This work was financed by the National Key R&D Program of China (2018YFD1000407), LiaoNing Revitalization Talents Program (XLYC2002052), Shenyang Innovation Program of Seed Industry (21-110-3-12), and the earmarked fund for CARS (CARS-23).

Author contributions

X.Y.F. and H.M.S. conceived and designed the experiments. X.M.Z. was involved in VIGS and data analysis. L.L.F. was involved in genetic transformation. M.L., Y.Y., and C.X.W. assisted the authors in data collation and analysis. All of the authors read and approved the final manuscript.

Data availability

The data supporting the findings of this study are available from the corresponding author upon request.

Conflict of interest

The authors declare no conflicts of interest in the submission of this manuscript.

References

[1]

Li X, Wang C, Cheng J et al. Transcriptome analysis of carbohydrate metabolism during bulblet formation and development in Lilium davidii var. unicolor. BMC Plant Biol. 2014; 14: 358.

[2]

Liu X, Wang Q, Gu J et al. Vernalization of oriental hybrid lily ’Sorbonne’: changes in physiology metabolic activity and molecular mechanism. Mol Biol Rep. 2014; 41: 6619-34.

[3]

Sun H, Silva JT, Li Y et al. Effects of low temperature on dormancy release in lily bulbs. Floricult Ornament Biotechnol. 2007; 1: 41-5.

[4]

Fan X, Yang Y, Li M et al. Transcriptomics and targeted metabolomics reveal the regulatory network of Lilium davidii var. unicolor during bulb dormancy release . Planta 2021; 254: 59.

[5]

Zhou Y, Wang W, Yang L et al. Identification and expression analysis of microRNAs in response to dormancy release during cold storage of Lilium pumilum bulbs . J Plant Growth Regul. 2021; 40: 388-404.

[6]

Sun H, Li T, Li Y . Changes of endogenous hormones in Lilium davidii var. unicolor bulbs during bulb development and storage at low temperature for dormancy release . Bull Bot Res. 2006; 26: 570-6.

[7]

Wang W, Su X, Tian Z et al. Transcriptome profiling provides insights into dormancy release during cold storage of Lilium pumilum. BMC Genomics. 2018; 19: 196.

[8]

Liu J, Sherif SM . Hormonal orchestration of bud dormancy cycle in deciduous woody perennials. Front Plant Sci. 2019; 10: 1136.

[9]

Wu J, Jin Y, Liu C et al. GhNAC83 inhibits corm dormancy release by regulating ABA signaling and cytokinin biosynthesis in Gladiolus hybridus. J Exp Bot. 2019; 70: 1221-37.

[10]

Sun Q, Zhang B, Yang C et al. Jasmonic acid biosynthetic genes TgLOX4 and TgLOX5 are involved in daughter bulb development in tulip (Tulipa gesneriana). Hortic Res. 2022; 9: uhac006.

[11]

Wang D, Gao Z, Du P et al. Expression of ABA metabolism-related genes suggests similarities and differences between seed dormancy and bud dormancy of peach (Prunus persica). Front Plant Sci. 2015; 6: 1248.

[12]

Li J, Xu Y, Liu Q et al. Abscisic acid (ABA) promotes the induction and maintenance of pear (Pyrus pyrifolia white pear group) flower bud endodormancy . Int J Mol Sci. 2018; 19: 310.

[13]

Vimont N, Fouché M, Campoy JA et al. From bud formation to flowering: transcriptomic state defines the cherry developmental phases of sweet cherry bud dormancy. BMC Genomics. 2019; 20: 974.

[14]

Moon J, Park CH, Son SH et al. Endogenous level of abscisic acid down-regulated by brassinosteroids signaling via BZR1 to control the growth of Arabidopsis thaliana. Plant Signal Behav. 2021; 16: 1926130.

[15]

Velappan Y, Chabikwa TG, Considine JA et al. The bud dormancy disconnect: latent buds of grapevine are dormant during summer despite a high metabolic rate. J Exp Bot. 2022; 73: 2061-76.

[16]

Barreto LC, Herken DMD, Silva BMR et al. ABA and GA4 dynamic modulates secondary dormancy and germination in Syngonanthus verticillatus seeds . Planta. 2020; 251: 86.

[17]

Ali F, Qanmber G, Li F et al. Updated role of ABA in seed maturation, dormancy, and germination. J Adv Res. 2022; 35: 199-214.

[18]

Ruttink T, Arend M, Morreel K et al. A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell. 2007; 19: 2370-90.

[19]

Han G, Qiao Z, Li Y et al. RING zinc finger proteins in plant abiotic stress tolerance. Front Plant Sci. 2022; 13: 877011.

[20]

Brugiere N, Zhang W, Xu Q et al. Overexpression of RING domain E3 ligase ZmXerico1 confers drought tolerance through regulation of ABA homeostasis. Plant Physiol 2017; 175: 1350-69.

[21]

Ko J, Yang S, Han K . Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis . Plant J. 2006; 47: 343-55.

[22]

Zeng DE, Hou P, Xiao F et al. Overexpression of Arabidopsis XERICO gene confers enhanced drought and salt stress tolerance in rice (Oryza sativa L.). J Plant Biochem Biotechnol. 2015; 24: 56-64.

[23]

Kim MH, Cho JS, Park EJ et al. Overexpression of a poplar RING-H2 zinc finger, Ptxerico, confers enhanced drought tolerance via reduced water loss and ion leakage in Populus. Int J Mol Sci. 2020; 21: 9454.

[24]

Vonapartis E, Mohamed D, Li J et al. CBF4/DREB1D represses XERICO to attenuate ABA, osmotic and drought stress responses in Arabidopsis. Plant J. 2022; 110: 961-77.

[25]

Xu H, Lantzouni O, Bruggink T et al. A molecular signal integration network underpinning Arabidopsis seed germination . Curr Biol. 2020; 30: 3703-3712.e4.

[26]

Yan R, Wang Z, Ren Y et al. Establishment of efficient genetic transformation systems and application of CRISPR/Cas9 genome editing technology in Lilium pumilum DC. Fisch. and Lilium longiflorum White Heaven . Int J Mol Sci. 2019; 20: 2920.

[27]

Hu Y, Han X, Yang M et al. The transcription factor INDUCER OF CBF EXPRESSION1 interacts with ABSCISIC ACID INSENSITIVE5 and DELLA proteins to fine-tune abscisic acid signaling during seed germination in Arabidopsis. Plant Cell. 2019; 31: 1520-38.

[28]

Shu K, Liu X, Xie Q et al. Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant. 2016; 9: 34-45.

[29]

Liu X, Hu P, Huang M et al. The NF-YC-RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nat Commun. 2016; 7: 12768.

[30]

Gomez-Soto D, Allona I, Perales M et al. FLOWERING LOCUS T2 promotes shoot apex development and restricts internode elongation via the 13-hydroxylation gibberellin biosynthesis pathway in poplar. Front Plant Sci. 2022; 12: 814195.

[31]

Sano N, Marion-Poll A . ABA metabolism and homeostasis in seed dormancy and germination. Int J Mol Sci. 2021; 22: 5069.

[32]

Du K, Zhao W, Mao Y et al. Maize ear growth is stimulated at the fourth day after pollination by cell wall remodeling and changes in lipid and hormone signaling. J Sci Food Agric. 2022; 102: 5429-39.

[33]

Li J, Seng S, Li D et al. Antagonism between abscisic acid and gibberellin regulates starch synthesis and corm development in Gladiolus hybridus. Hortic Res. 2021; 8: 155.

[34]

Gianinetti A . In dormant red rice seeds, the inhibition of early seedling growth, but not of germination, requires extracellular ABA. Plants (Basel). 2022; 11: 1023.

[35]

Zheng C, Halaly T, Acheampong AK et al. Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot. 2015; 66: 1527-42.

[36]

Parker ML, Clark MB, Campbell C . Abscisic acid applications in peach. Acta Hortic. 2012; 962: 403-9.

[37]

Malek M, Ghaderi-Far F, Torabi B et al. Dynamics of seed dormancy and germination at high temperature stress is affected by priming and phytohormones in rapeseed (Brassica napus L.). J Plant Physiol. 2022; 269: 153614.

[38]

Goggin DE, Steadman KJ, Emery RJN et al. ABA inhibits germination but not dormancy release in mature imbibed seeds of Lolium rigidum Gaud. J Exp Bot. 2009; 60: 3387-96.

[39]

Gianinetti A, Vernieri P . On the role of abscisic acid in seed dormancy of red rice. J Exp Bot. 2007; 58: 3449-62.

[40]

Awan SZ, Chandler JO, Harrison PJ et al. Promotion of germination using hydroxamic acid inhibitors of 9-cis-epoxycarotenoid dioxygenase. Front Plant Sci. 2017; 8: 357.

[41]

Chauffour F, Bailly M, Perreau F et al. Multi-omics analysis reveals sequential roles for ABA during seed maturation. Plant Physiol. 2019; 180: 1198-218.

[42]

Ren L, Zhao H, Liu XY et al. Transcriptome reveals roles of lignin-modifying enzymes and abscisic acid in the symbiosis of Mycena and Gastrodia elata. Int J Mol Sci. 2021; 22: 6557.

[43]

Okamoto M, Kuwahara A, Seo M et al. CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol. 2006; 141: 97-107.

[44]

Matakiadis T, Alboresi A, Jikumaru Y et al. The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy . Plant Physiol. 2009; 149: 949-60.

[45]

Wu J, Seng S, Sui J et al. Gladiolus hybridus ABSCISIC ACID INSENSITIVE 5 (GhABI5) is an important transcription factor in ABA signaling that can enhance Gladiolus corm dormancy and Arabidopsis seed dormancy . Front Plant Sci. 2015; 6: 960.

[46]

Née G, Kramer K, Nakabayashi K et al. DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nat Commun. 2017; 8: 72.

[47]

Nishimura N, Tsuchiya W, Moresco JJ et al. Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme. Nat Commun 2018; 9: 2132.

[48]

Gao Y, Li H, Deng D et al. Characterization and expression analysis of the maize RING-H2 finger protein gene ZmXERICO responsive to plant hormones and abiotic stresses. Acta Physiol Plant. 2012; 34: 1529-35.

[49]

Cho SK, Ryu MY, Kim JH et al. RING E3 ligases: key regulatory elements are involved in abiotic stress responses in plants. BMB Rep. 2017; 50: 393-400.

[50]

Shu K, Yang W . E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant Cell Physiol. 2017; 58: 1461-76.

[51]

Lee H, Xiong L, Gong Z et al. The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning . Genes Dev. 2001; 15: 912-24.

[52]

Chen M, Ni M . RFI2, a RING-domain zinc finger protein, negatively regulates CONSTANS expression and photoperiodic flowering. Plant J. 2006; 46: 823-33.

[53]

Jmii S, Cappadocia L . Plant SUMO E3 ligases: function, structural organization, and connection with DNA. Front Plant Sci. 2021; 12: 652170.

[54]

Zentella R, Zhang ZL, Park M et al. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell. 2007; 19: 3037-57.

[55]

Ariizumi T, Hauvermale AL, Nelson SK et al. Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling . Plant Physiol. 2013; 162: 2125-39.

[56]

Shi Y, Ding Y, Yang S . Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 2018; 23: 623-37.

[57]

Liu J, Li J, Fu C et al. Comparative physiology and transcriptome analysis reveals the regulatory mechanism of genome duplication enhancing cold resistance in Fragaria nilgerrensis. Environ Exp Bot. 2021; 188: 104509.

[58]

Song S, Yan R, Wang C et al. Improvement of a genetic transformation system and preliminary study on the function of LpABCB21 and LpPILS7 based on somatic embryogenesis in Lilium pumilum DC. Fisch. Int J Mol Sci. 2020; 21: 6784.

[59]

Clough SJ, Bent AF . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998; 16: 735-43.

[60]

Yan R, Song S, Li H et al. Functional analysis of the eTM-miR171-SCL6 module regulating somatic embryogenesis in Lilium pumilum DC. Fisch. Hortic Res. 2022; 9: uhac045.

[61]

Wu J, Wu W, Liang J et al. GhTCP19 transcription factor regulates corm dormancy release by repressing GhNCED expression in Gladiolus. Plant Cell Physiol. 2019; 60: 52-62.

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