Auxin regulates bulbil initiation by mediating sucrose metabolism in Lilium lancifolium

Yin Xin , Xi Chen , Jiahui Liang , Shaokun Wang , Wenqiang Pan , Jingxiang Wu , Mingfang Zhang , Michele Zaccai , Xiaonan Yu , Xiuhai Zhang , Jian Wu , Yunpeng Du

Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) : 054

PDF (3844KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) :054 DOI: 10.1093/hr/uhae054
Articles
research-article
Auxin regulates bulbil initiation by mediating sucrose metabolism in Lilium lancifolium
Author information +
History +
PDF (3844KB)

Abstract

Lily bulbils, which serve as advantageous axillary organs for vegetative propagation, have not been extensively studied in terms of the mechanism of bulbil initiation. The functions of auxin and sucrose metabolism have been implicated in axillary organ development, but their relationship in regulating bulbil initiation remains unclear. In this study, exogenous indole-3-acetic acid (IAA) treatment increased the endogenous auxin levels at leaf axils and significantly decreased bulbil number, whereas treatment with the auxin polar transport inhibitor N-1-naphthylphthalamic acid (NPA), which resulted in a low auxin concentration at leaf axils, stimulated bulbil initiation and increased bulbil number. A low level of auxin caused by NPA spraying or silencing of auxin biosynthesis genes YUCCA FLAVIN MONOOXYGENASE-LIKE 6 (LlYUC6) and TRYPTOPHAN AMINOTRANSFERASE RELATED 1 (LlTAR1) facilitated sucrose metabolism by activating the expression of SUCROSE SYNTHASES 1 (LlSusy1) and CELL WALL INVERTASE 2 (LlCWIN2), resulting in enhanced bulbil initiation. Silencing LlSusy1 or LlCWIN2 hindered bulbil initiation. Moreover, the transcription factor BASIC HELIX-LOOP-HELIX 35 (LlbHLH35) directly bound the promoter of LlSusy1, but not the promoter of LlCWIN2, and activated its transcription in response to the auxin content, bridging the gap between auxin and sucrose metabolism. In conclusion, our results reveal that an LlbHLH35-LlSusy1 module mediates auxin-regulated sucrose metabolism during bulbil initiation.

Cite this article

Download citation ▾
Yin Xin, Xi Chen, Jiahui Liang, Shaokun Wang, Wenqiang Pan, Jingxiang Wu, Mingfang Zhang, Michele Zaccai, Xiaonan Yu, Xiuhai Zhang, Jian Wu, Yunpeng Du. Auxin regulates bulbil initiation by mediating sucrose metabolism in Lilium lancifolium. Horticulture Research, 2024, 11 (4) : 054 DOI:10.1093/hr/uhae054

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 32371954 and 32171864 to Y.D.; 32372740 and 32172617 to J.W.; 32302599 to J.L.), the Excellent Youth Science Foundation of Beijing Academy of Agriculture and Forestry Sciences (YXQN202303 to Y.D.), Pinduoduo-China Agricultural University Research Fund (PC2023B02009), Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects (CEFF-PXM 2019_014207_000032), and the 2115 Talent Development Program of China Agricultural University, the Strategic Development Department of China Association for Science and Technology, 111 Project of the Ministry of Education (B17043), and China Postdoctoral Science Foundation (2023M740311).

Author contributions

X.C. and Y.X. observed the development of bulbil and performed the endogenous hormone treatments; Y.X. and W.P. conducted the transcriptome analysis; X.C., Y.X., and S.W. performed gene silencing; Y.X., J.X.W., and M.F.Z. conducted the metabolite analysis; X.C., Y.X., J.L, J.W., and M.Z. wrote and rewrote the article; J.W., Y.D., X.Y., X.C., J.L., and X.Z. conceived the study and reviewed the article; all authors read and approved the article.

Data availability statement

The raw sequence data of RNA-seq reported in this study have been deposited in the NCBI SRA data under accession number PRJNA916842. The authors declare that all data supporting the findings of this study are available from within the article and supplementary data or are available upon reasonable request from the corresponding author.

Conflict of interest

The authors report no declarations of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

References

[1]

Du YP, He HB, Wang ZX. et al. Investigation and evaluation of the genus Lilium resources native to China. Genet Resour Crop Evol. 2014; 61:395-412

[2]

Mi YC, López-Pujol J, Chung JM. et al. Polyploidy in Lilium lancifolium: evidence of autotriploidy and no niche divergence between diploid and triploid cytotypes in their native ranges. Flora. 2015; 213:57-68

[3]

Yang PP, Xu LF, Xu H. et al. Morphological and anatomical observation during the formation of bulbils in Lilium lancifolium. Caryologia. 2018; 71:146-9

[4]

Teale WD, Paponov IA, Palme K. Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol. 2006; 7:847-59

[5]

Wang Y, Jiao Y. Axillary meristem initiation—a way to branch out. Curr Opin Plant Biol. 2018; 41:61-6

[6]

Yang M, Jiao Y. Regulation of axillary meristem initiation by transcription factors and plant hormones. Front Plant Sci. 2016; 7:183

[7]

Yang T, Jiao Y, Wang Y. Stem cell basis of shoot branching. Plant Cell Physiol. 2023; 64:291-6

[8]

Vernoux T, Brunoud G, Farcot E. et al. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol. 2011; 7:508

[9]

Wang Y, Wang J, Shi B. et al. The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. Plant Cell. 2014; 26:2055-67

[10]

Dai Y, Luo L, Zhao Z. Genetic robustness control of auxin output in priming organ initiation. Proc Natl Acad Sci USA. 2023; 120:e2221606120

[11]

Hofmann NR. YUC and TAA1/TAR proteins function in the same pathway for auxin biosynthesis. Plant Cell. 2011; 23:3869-9

[12]

Meng WJ, Cheng ZJ, Sang YL. et al. Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell. 2017; 29:1357-72

[13]

Thelander M, Landberg K, Muller A. et al. Apical dominance control by TAR-YUC-mediated auxin biosynthesis is a deep homology of land plants. Curr Biol. 2022; 32:3838-3846.e5

[14]

Lv X, Zhang M, Li X. et al. Transcriptome profiles reveal the crucial roles of auxin and cytokinin in the "shoot branching" of Cremastra appendiculata. Int J Mol Sci. 2018; 19:3354

[15]

Tamas IA, Schlossberg-Jacobs JL, Lim R. et al. Effect of plant growth substances on the growth of axillary buds in cultured stem segments of Phaseolus vulgaris L. Plant Growth Regul. 1989; 8:165-83

[16]

Wu ZG, Jiang W, Tao ZM. et al.Morphological and stage-specific transcriptome analyses reveal distinct regulatory programs underlying yam (Dioscorea alata L.) bulbil growth. J Exp Bot. 2020; 71:1899-914

[17]

Li J, Sun M, Li H. et al. Full-length transcriptome-referenced analysis reveals crucial roles of hormone and wounding during induction of aerial bulbils in lily. BMC Plant Biol. 2022; 22:415

[18]

Tanimoto S, Matsubara Y. Stimulating effect of spermine on bulblet formation in bulb-scale segments of Lilium longiflorum. Plant Cell Rep. 1995; 15:297-300

[19]

Nägele T, Gibon Y, Le Hir R. Plant sugar metabolism, transport and signalling in challenging environments. Physiol Plant. 2022; 174:e13768

[20]

Braun DM. Phloem loading and unloading of sucrose: what a long, strange trip from source to sink. Annu Rev Plant Biol. 2022; 73:553-84

[21]

Duan Y, Yang L, Zhu H. et al. Structure and expression analysis of sucrose phosphate synthase, sucrose synthase and invertase gene families in Solanum lycopersicum. Int J Mol Sci. 2021; 22:4698

[22]

Koch K. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol. 2004; 7:235-46

[23]

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

[24]

Ren ZM, Zhang D, Jiao C. et al. Comparative transcriptome and metabolome analyses identified the mode of sucrose degradation as a metabolic marker for early vegetative propagation in bulbs of Lycoris. Plant J. 2022; 112:115-34

[25]

Liao S, Wang L, Li J. et al. Cell wall Invertase is essential for ovule development through sugar signaling rather than provision of carbon nutrients. Plant Physiol. 2020; 183:1126-44

[26]

Ruan YL. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol. 2014; 65:33-67

[27]

Patil SB, Barbier FF, Zhao J. et al. Sucrose promotes D53 accumulation and tillering in rice. New Phytol. 2022; 234:122-36

[28]

Liang JH, Li JR, Liu C. et al. GhbZIP30-GhCCCH17 module accelerates corm dormancy release by reducing endogenous ABA under cold storage in Gladiolus. Plant Cell Environ. 2023; 46:2078-96

[29]

Tsai AY, Gazzarrini S. Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture. Front Plant Sci. 2014; 5:119

[30]

Luo Z, Janssen BJ, Snowden KC. The molecular and genetic regulation of shoot branching. Plant Physiol. 2021; 187:1033-44

[31]

Adamowski M, Friml J. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell. 2015; 27:20-32

[32]

Strader L, Weijers D, Wagner D. Plant transcription factors—being in the right place with the right company. Curr Opin Plant Biol. 2022; 65:102136

[33]

Hao Y, Zong X, Ren P. et al. Basic helix-loop-helix (bHLH) transcription factors regulate a wide range of functions in Arabidopsis. Int J Mol Sci. 2021; 22:7152

[34]

Liang J, Wu Z, Zheng J. et al. The GATA factor HANABA TARANU promotes runner formation by regulating axillary bud initiation and outgrowth in cultivated strawberry. Plant J. 2022; 110:1237-54

[35]

Ruegger M, Dewey E, Hobbie L. et al. Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell. 1997; 9:745-57

[36]

Barbier FF, Dun EA, Beveridge CA. Apical dominance. Curr Biol. 2017; 27:R864-r865

[37]

Lunn JE. Sucrose metabolism. eLS. 2016;1-9

[38]

Mroue S, Simeunovic A, Robert HS. Auxin production as an integrator of environmental cues for developmental growth regulation. J Exp Bot. 2018; 69:201-12

[39]

Wang Q, Kohlen W, Rossmann S. et al. Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. Plant Cell. 2014; 26:2068-79

[40]

Abas L, Kolb M, Stadlmann J. et al. Naphthylphthalamic acid associates with and inhibits PIN auxin transporters. Proc Natl Acad Sci USA. 2021; 118:e2020857118

[41]

Serrani JC, Carrera E, Ruiz-Rivero O. et al. Inhibition of auxin transport from the ovary or from the apical shoot induces parthenocarpic fruit-set in tomato mediated by gibberellins. Plant Physiol. 2010; 153:851-62

[42]

Luo P, Di DW. Precise regulation of the TAA1/TAR-YUCCA auxin biosynthesis pathway in plants. Int J Mol Sci. 2023; 24:8514

[43]

Marinangeli PA, Hernández LF, Pellegrini CP. et al. Bulblet differentiation after scale propagation of Lilium longiflorum. J Am Soc Hortic Sci. 2003; 128:324-9

[44]

Yang PP, Xu L, Xu H. et al. Histological and transcriptomic analysis during bulbil formation in Lilium lancifolium. Front Plant Sci. 2017; 8:1508

[45]

Liang J, Chen Y, Hou J. et al. Cytokinins influence bulblet formation by modulating sugar metabolism and endogenous hormones in Asiatic hybrid lily. Ornamental Plant Res 2023;3:19.

[46]

Ren Y, Liao S, Xu Y. An update on sugar allocation and accumulation in fruits. Plant Physiol. 2023; 193:888-99

[47]

Meng LS, Bao QX, Mu XR. et al. Glucose-and sucrose-signaling modules regulate the Arabidopsis juvenile-to-adult phase transition. Cell Rep. 2021; 36:109348

[48]

Salam BB, Barbier F, Danieli R. et al. Sucrose promotes stem branching through cytokinin. Plant Physiol. 2021; 185:1708-21

[49]

Tao X, Wu Q, Fu X. et al. Understanding of exogenous auxin in regulating sucrose metabolism during postharvest tomato fruit ripening. Postharvest Biol Technol. 2022; 189:111913

[50]

Li J, Foster R, Ma S. et al. Identification of transcription factors controlling cell wall invertase gene expression for reproductive development via bioinformatic and transgenic analyses. Plant J. 2021; 106:1058-74

[51]

Zhao Z, Wang C, Yu X. et al. Auxin regulates source-sink carbohydrate partitioning and reproductive organ development in rice. Proc Natl Acad Sci USA. 2022; 119:e2121671119

[52]

Kim S, Hwang G, Kim S. et al. The epidermis coordinates thermoresponsive growth through the phyB-PIF4-auxin pathway. Nat Commun. 2020; 11:1053

[53]

Jiang C, Liang Y, Deng S. et al. The RhLOL1-RhILR3 module mediates cytokinin-induced petal abscission in rose. New Phytol. 2023; 237:483-96

[54]

Yu JQ, Gu KD, Zhang LL. et al. MdbHLH3 modulates apple soluble sugar content by activating phosphofructokinase gene expression. J Integr Plant Biol. 2022; 64:884-900

[55]

Xu T, Fu D, Xiong X. et al. OsbHLH067, OsbHLH068, and OsbHLH069 redundantly regulate inflorescence axillary meristem formation in rice. PLoS Genet. 2023; 19:e1010698

[56]

Wu J, Seng S, Sui J. et al. Gladiolus hybridus ABSCISIC ACID INSENSITIVE 5 (Gh ABI5) is an important transcription factor in ABA signaling that can enhance Gladiolus corm dormancy and Arabidopsis seed dormancy. Front Plant Sci. 2015; 6:960

[57]

Chen Y, Dan Z, Li S. Measuring endogenous GA and IAA. Bio Protoc. 2022; 184:393-406

[58]

Farrow SC, Emery RN. Concurrent profiling of indole-3-acetic acid, abscisic acid, and cytokinins and structurally related purines by high-performance-liquid-chromatography tandem electrospray mass spectrometry. Plant Methods. 2012; 8:42-18

[59]

Liang Y, Jiang C, Liu Y. et al. Auxin regulates sucrose transport to repress petal abscission in rose (Rosa hybrida). Plant Cell. 2020; 32:3485-99

[60]

Podnar J, Deiderick H, Huerta G. et al. Next-generation sequencing RNA-Seq library construction. Curr Protoc Mol Biol. 2014; 106:4.21.1-19

[61]

Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15:550

[62]

Mao X, Cai T, Olyarchuk JG. et al. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics. 2005; 21:3787-93

[63]

Zhang J, Gai MZ, Xue BY. et al. The use of miRNAs as reference genes for miRNA expression normalization during Lilium somatic embryogenesis by real-time reverse transcription PCR analysis. Plant Cell Tiss Org. 2017; 129:105-18

[64]

Chong L, Xu R, Huang P. et al. The tomato OST1-VOZ1 module regulates drought-mediated flowering. Plant Cell. 2022; 34:2001-18

[65]

Zhang Y, Wu Z, Feng M. et al. The circadian-controlled PIF8-BBX28 module regulates petal senescence in rose flowers by governing mitochondrial ROS homeostasis at night. Plant Cell. 2021; 33:2716-35

PDF (3844KB)

85

Accesses

0

Citation

Detail

Sections
Recommended

/