Metabolome profiling of stratified seeds provides insight into the regulation of dormancy in Davidia involucrata

doi:10.1016/j.pld.2021.12.001

Plant Diversity ›› 2022, Vol. 44 ›› Issue (04): 417-427.DOI: 10.1016/j.pld.2021.12.001

• Articles • 上一篇

Metabolome profiling of stratified seeds provides insight into the regulation of dormancy in Davidia involucrata

Shiming Deng^a,b, Qiang Xiao^a, Cigui Xu^a, Jian Hong^a, Zhijun Deng^a, Dan Jiang^a, Shijia Luo^a

a Key Laboratory of Biologic Resources Protection and Utilization of Hubei Province, Hubei Minzu University, Enshi 445000, Hubei Province, China;
b Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China

收稿日期:2021-08-17 修回日期:2021-11-20 出版日期:2022-07-25 发布日期:2022-08-13
通讯作者: Shijia Luo,E-mail:1988002@humzu.edu.cn
基金资助:
This work was funded by the National Natural Sciences Foundation of China (31460203, 31860073) and Research Center for Germplasm Engineering of Characteristic Plant Resources in Enshi Prefecture (2019e2021). Hubei Key Laboratory of Biological Resources Protection and Utilization (PT012204).

Metabolome profiling of stratified seeds provides insight into the regulation of dormancy in Davidia involucrata

Shiming Deng^a,b, Qiang Xiao^a, Cigui Xu^a, Jian Hong^a, Zhijun Deng^a, Dan Jiang^a, Shijia Luo^a

a Key Laboratory of Biologic Resources Protection and Utilization of Hubei Province, Hubei Minzu University, Enshi 445000, Hubei Province, China;
b Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China

Received:2021-08-17 Revised:2021-11-20 Online:2022-07-25 Published:2022-08-13
Contact: Shijia Luo,E-mail:1988002@humzu.edu.cn
Supported by:
This work was funded by the National Natural Sciences Foundation of China (31460203, 31860073) and Research Center for Germplasm Engineering of Characteristic Plant Resources in Enshi Prefecture (2019e2021). Hubei Key Laboratory of Biological Resources Protection and Utilization (PT012204).

摘要/Abstract

摘要： Dove tree (Davidia involucrata), a tertiary vestige species, is well-adapted to cool conditions. Dormancy in D. involucrata seed lasts for an extremely long period of time, typically between 3 and 4 years, and this characteristic makes the species an excellent model for studying the mechanisms of seed dormancy. The molecular mechanisms governing germination control in D. involucrata are still unknown. Seed stratification have been reported to enhance germination in recalcitrant seeds. We performed a widely targeted metabolome profiling to identify metabolites and associated pathways in D. involucrata seeds from six different moist sand stratification durations (0-30 months) using the ultra-high-performance liquid chromatography-Q Exactive Orbitrap-Mass spectrometry. There was an increasing germination rate with prolonged stratification durations (12-30 months). Furthermore, we detected 10,008 metabolites in the stratified seeds. We also detected 48 differentially accumulated metabolites (DAMs) between all stratification periods in the seeds, with 10 highly conserved metabolites. Most of the differentially accumulated metabolites between unstratified and stratified seeds were enriched in purine metabolism, pyrimidine metabolism, flavone and flavonol biosynthesis, phenylpropanoid biosynthesis, and arginine biosynthesis pathways. Key phytohormones, abscisic acid, indole-3 acetic acid, and sinapic acid were differentially accumulated in the seeds and are predicted to regulate dormancy in D. involucrata. We have provided extensive metabolic information useful for future works on dove tree germination study.

关键词: Dove tree, Metabolome, Dormancy, Abscisic acid, Stratification

Abstract: Dove tree (Davidia involucrata), a tertiary vestige species, is well-adapted to cool conditions. Dormancy in D. involucrata seed lasts for an extremely long period of time, typically between 3 and 4 years, and this characteristic makes the species an excellent model for studying the mechanisms of seed dormancy. The molecular mechanisms governing germination control in D. involucrata are still unknown. Seed stratification have been reported to enhance germination in recalcitrant seeds. We performed a widely targeted metabolome profiling to identify metabolites and associated pathways in D. involucrata seeds from six different moist sand stratification durations (0-30 months) using the ultra-high-performance liquid chromatography-Q Exactive Orbitrap-Mass spectrometry. There was an increasing germination rate with prolonged stratification durations (12-30 months). Furthermore, we detected 10,008 metabolites in the stratified seeds. We also detected 48 differentially accumulated metabolites (DAMs) between all stratification periods in the seeds, with 10 highly conserved metabolites. Most of the differentially accumulated metabolites between unstratified and stratified seeds were enriched in purine metabolism, pyrimidine metabolism, flavone and flavonol biosynthesis, phenylpropanoid biosynthesis, and arginine biosynthesis pathways. Key phytohormones, abscisic acid, indole-3 acetic acid, and sinapic acid were differentially accumulated in the seeds and are predicted to regulate dormancy in D. involucrata. We have provided extensive metabolic information useful for future works on dove tree germination study.

Key words: Dove tree, Metabolome, Dormancy, Abscisic acid, Stratification

Shiming Deng, Qiang Xiao, Cigui Xu, Jian Hong, Zhijun Deng, Dan Jiang, Shijia Luo. Metabolome profiling of stratified seeds provides insight into the regulation of dormancy in Davidia involucrata[J]. Plant Diversity, 2022, 44(04): 417-427.

参考文献

Ali, F., Qanmber, G., Li, F., et al., 2021. Updated role of ABA in seed maturation, dormancy, and germination. J. Adv. Res. https://doi.org/10.1016/j.jare.2021.03. 011.
Ali Reza Einali, H.R.S., 2007. Alleviation of dormancy in walnut kernels. Tree Physiol. 27, 519-525.
Apte, P.v., Laloraya, M.M., 1982. Inhibitory action of phenolic compounds on abscisic acid-induced abscission. J. Exp. Bot. 33, 826-830. https://doi.org/10.1093/jxb/ 33.4.826.
Arc, E., Chibani, K., Grappin, P., et al., 2012. Cold stratification and exogenous nitrates entail similar functional proteome adjustments during Arabidopsis seed dormancy release. J. Proteome Res. 11, 5418-5432. https://doi.org/10.1021/pr3006815.
Bi, B., Tang, J., Han, S., et al., 2017. Sinapic acid or its derivatives interfere with abscisic acid homeostasis during Arabidopsis thaliana seed germination. BMC Plant Biol. 17. https://doi.org/10.1186/s12870-017-1048-9.
Brady, S.M., Sarkar, S.F., Bonetta, D., et al., 2003. The ABSCISIC ACID INSENSITIVE 3(ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. Plant J. 34, 67-75. https://doi.org/10.1046/j.1365-313X.2003.01707.x.
Cadman, C.S.C., Toorop, P.E., Hilhorst, H.W.M., et al., 2006. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 46, 805-822. https://doi.org/10.1111/j.1365-313X.2006.02738.x.
Chen, Z., Cao, X., Niu, J., 2021. Effects of exogenous ascorbic acid on seed germination and seedling salt-tolerance of alfalfa. PLoS One 16, e0250926. https://doi.org/10.1371/JOURNAL.PONE.0250926.
Cornelius, S., Witz, S., Rolletschek, H., et al., 2011. Pyrimidine degradation influences germination seedling growth and production of Arabidopsis seeds. J. Exp. Bot. 62, 5623-5632. https://doi.org/10.1093/jxb/err251.
Das, A., Kim, D.W., Khadka, P., et al., 2017. Unraveling key metabolomic alterations in wheat embryos derived from freshly harvested and water-imbibed seeds of two wheat cultivars with contrasting dormancy status. Front. Plant Sci. 8, 1203. https://doi.org/10.3389/fpls.2017.01203.
Debeaujon, I., Léon-Kloosterziel, K.M., Koornneef, M., 2000. Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122, 403-413. https://doi.org/10.1104/pp.122.2.403.
Debeaujon, I., Nesi, N., Perez, P., et al., 2003. Proanthocyanidin-accumulating cells in arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15, 2514-2531. https://doi.org/10.1105/tpc.014043.
Downie, B., Bewley, J.D., 2000. Soluble sugar content of white spruce (Picea glauca) seeds during and after germination. Physiol. Plantarum 110, 1-12. https://doi.org/10.1034/j.1399-3054.2000.110101.x.
El-Araby, M.M., Moustafa, S.M.A., Ismail, A.I., et al., 2006. Hormone and phenol levels during germination and osmopriming of tomato seeds, and associated variations in protein patterns and anatomical seed features. Acta Agron. Hung. 54, 441-457. https://doi.org/10.1556/AAgr.54.2006.4.7.
Finch-Savage, W.E., Leubner-Metzger, G., 2006. Seed dormancy and the control of germination. New Phytol. 171, 501-523. https://doi.org/10.1111/j.1469-8137.2006.01787.x.
Gang, W., Shan-heng, H., Hong-chang, W., et al., 2004. Living characteristics of rare and endangered species dDavidia involucrata. J. For. Res. 15, 39-44. https://doi.org/10.1007/bf02858008.
Gao, F., Jordan, M.C., Ayele, B.T., 2012. Transcriptional programs regulating seed dormancy and its release by after-ripening in common wheat (Triticum aestivum L.). Plant Biotechnol. J. 10, 465-476. https://doi.org/10.1111/j.1467-7652.2012.00682.x.
Gianinetti, A., Finocchiaro, F., Bagnaresi, P., et al., 2018. Seed dormancy involves a transcriptional program that supports early plastid functionality during imbibition. Plants 7, 35. https://doi.org/10.3390/plants7020035.
Hance, B.A., Bevington, J.M., 1992. Changes in protein synthesis during stratification and dormancy release in embryos of sugar maple (Acer saccharum). Physiol. Plantarum 86, 365-371. https://doi.org/10.1111/j.1399-3054.1992.tb01332.x.
Guillamón, J.G., Prudencio, Á.S., Yuste, J.E., et al., 2020. Ascorbic acid and prunasin, two candidate biomarkers for endodormancy release in almond flower buds identified by a nontargeted metabolomic study. Hortic. Res. 7, 1-13. https://doi.org/10.1038/s41438-020-00427-5.
Han, C., Yang, P., 2015. Studies on the molecular mechanisms of seed germination. Proteomics 15, 1671-1679. https://doi.org/10.1002/pmic.201400375.
He, Z.C., Li, J.Q., Wang, H.C., 2004. Karyomorphology of Davidia involucrata and Camptotheca acuminata, with special reference to their systematic positions. Bot. J. Linn. Soc. 144, 193-198. https://doi.org/10.1111/j.1095-8339.2003.00241.x.
Hilhorst, H.W.M., 1995. A critical update on seed dormancy. I. Primary dormancy. Seed Sci. Res. 5, 61-73. https://doi.org/10.1017/S0960258500002634.
Jaganathan, G.K., 2020. Defining correct dormancy class matters : morphological and morphophysiological dormancy in Arecaceae. Ann. For. Sci. 77, 100. https://doi.org/10.1007/s13595-020-01010-7.
Jiang, Z., Xu, G., Jing, Y., et al., 2016. Phytochrome B and REVEILLE1/2-mediated signalling controls seed dormancy and germination in Arabidopsis. Nat. Commun. 7, 1-10. https://doi.org/10.1038/ncomms12377.
Kanehisa, M., Goto, S., 2000. KEGG: Kyoto Encyclopedia of genes and Genomes. Nucleic Acids Res. 28, 27-30. https://doi.org/10.1093/nar/28.1.27.
Kong, D., Ju, C., Parihar, A., et al., 2015. Arabidopsis glutamate receptor homolog3.5 modulates cytosolic Ca²⁺ level to counteract effect of abscisic acid in seed germination. Plant Physiol. 167, 1630-1642. https://doi.org/10.1104/pp.114.251298.
Kucera, B., Cohn, M.A., Leubner-Metzger, G., 2005. Plant hormone interactions during seed dormancy release and germination. Seed Sci. Res. 15, 281-307. https://doi.org/10.1079/ssr2005218.
Li, A., Li, S., Wu, X., et al., 2016a. Effect of light intensity on leaf photosynthetic characteristics and accumulation of flavonoids in Lithocarpus litseifolius (Hance) Chun. (Fagaceae). Open J. For. 6, 445-459. https://doi.org/10.4236/ojf.2016.65034.
Li, Y.X., Chen, L., Juan, L., et al., 2002. Suppression subtractive hybridization cloning of cDNAs of differentially expressed genes in dovetree (Davidia involucrata) bracts. Plant Mol. Biol. Rep. 20, 231-238. https://doi.org/10.1007/BF02782458.
Li, M., Dong, X., Peng, J., et al., 2016b. De novo transcriptome sequencing and gene expression analysis reveal potential mechanisms of seed abortion in dove tree(Davidia involucrata Baill.). BMC Plant Biol. 16, 82. https://doi.org/10.1186/s12870-016-0772-x.
Li, B., Zhang, P., Wang, F., et al., 2021. Integrated analysis of the transcriptome and metabolome revealed candidate genes involved in ga3-induced dormancy release in Leymus chinensis seeds. Int. J. Mol. Sci. 22. https://doi.org/10.3390/ijms22084161.
Liu, R., Lu, J., Xing, J., Du, M., Wang, M., Zhang, L., Li, Y., Zhang, C., Wu, Y., 2021a. Transcriptome and metabolome analyses revealing the potential mechanism of seed germination in Polygonatum cyrtonema. Sci. Rep. 11. https://doi.org/10.1038/s41598-021-91598-1.
Liu, P.P., Montgomery, T.A., Fahlgren, N., et al., 2007. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 52, 133-146. https://doi.org/10.1111/j.1365-313X.2007.03218.x.
Liu, S., Yang, L., Li, Jialong, et al., 2021b. FHY3 interacts with phytochrome B and regulates seed dormancy and germination. Plant Physiol. https://doi.org/10.1093/plphys/kiab147.
Laloraya, M.M., Nozzolillo, C., Purohit, S., et al., 1986. Reversal of abscisic acidinduced stomatal closure by trans-cinnamic and p-coumaric acid. Plant Physiol. 81, 253-258. https://doi.org/10.1104/pp.81.1.253.
Liu, X., Zhang, H., Zhao, Y., et al., 2013. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 110, 15485-15490. https://doi.org/10.1073/pnas.1304651110.
Ma, Z., Bykova, N.v., Igamberdiev, A.U., 2017. Cell signaling mechanisms and metabolic regulation of germination and dormancy in barley seeds. Crop J. https://doi.org/10.1016/j.cj.2017.08.007.
Mares, D.J., Mrva, K., Cheong, J., et al., 2021. Dormancy and dormancy release in white-grained wheat (Triticum aestivum L.). Planta 253. https://doi.org/10.1007/s00425-020-03518-8.
Mesihovic, A., Iannacone, R., Firon, N., Fragkostefanakis, S., 2016. Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reprod. https://doi.org/10.1007/s00497-016-0281-y.
Mochida, K., Shinozaki, K., 2011. Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcr153.
Mock, H.P., Strack, D., 1993. Energetics of the uridine 50-diphosphoglucose:hydroxycinnamic acid acyl-glucosyltransferase reaction. Phytochemistry 32, 575-579. https://doi.org/10.1016/S0031-9422(00)95139-2.
Moffatt, B.A., Ashihara, H., 2002. Purine and pyrimidine nucleotide synthesis and metabolism. The Arabidopsis Book/American Society of Plant Biologists 1, e0018. https://doi.org/10.1199/TAB.0018.
Noland, T.L., Brad Murphy, J., 1986. Protein synthesis and aminopeptidase activity in dormant sugar pine seeds during stratification and warm incubation. J. Plant Physiol. 124, 1-10. https://doi.org/10.1016/S0176-1617(86)80172-9.
Park, C.J., Seo, Y.S., 2015. Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol. J. https://doi.org/10.5423/PPJ.RW.08.2015.0150.
Qi, G., Li, J.T., Ruan, Q.P., et al., 2009. An optimised, small-scale preparation of highquality RNA from dry seeds of Davidia involucrata. Phytochem. Anal. 20, 139-142. https://doi.org/10.1002/pca.1108.
Qiu, X.M., Sun, Y.Y., Ye, X.Y., et al., 2020. Signaling role of glutamate in plants. Front. Plant Sci. 10, 1743. https://doi.org/10.3389/fpls.2019.01743.
Roman, T.L., Galperin,M.Y.,Natale,D.A.,etal.,2000.The COG database:a tool for genomescale analysis of protein functions and evolution. Nucleic Acids Res. 28, 33-36.
Song, Y., Zhu, J., 2019. The roles of metabolic pathways in maintaining primary dormancy of Pinus koraiensis seeds. BMC Plant Biol. 19. https://doi.org/10.1186/s12870-019-2167-2.
Shimozu, Y., Kimura, Y., Esumi, A., et al., 2017. Ellagitannins of Davidia involucrata. I. Structure of davicratinic acid a and effects of davidia tannins on drug-resistant bacteria and human oral squamous cell carcinomas. Molecules 22. https://doi.org/10.3390/molecules22030470.
Song, Y., Zhu, J.J., 2016. How does moist cold stratification under field conditions affect the dormancy release of Korean pine seed (Pinus koraiensis)? Seed Sci. Technol. 44, 27-42. https://doi.org/10.15258/SST.2016.44.1.06.
Strack, D., 1981. Sinapine as a supply of choline for the biosynthesis of phosphatidylcholine in Raphanus sativus seedlings. Z. Naturforsch. C 36, 215-221. https://doi.org/10.1515/znc-1981-3-407.
Su, Z.X., Zhang, S.L., 1999. The reproductive phenology and the influencing factors of Davidia involucrata population. J. Coll. Sci. Teach. 20, 313-318.
Sun, J.F., Gong, Y.B., Renner, S.S., et al., 2008. Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae: Cornales): rain protection and pollinator attraction. Am. Nat. 171, 119-124. https://doi.org/10.1086/523953.
Szczotka, Z., Pawłowski, T., Krawiarz, K., 2003. Proteins and polyamines during dormancy breaking of European beech (Fagus sylvatica L.) seeds. Acta Physiol. Plant. 25, 423-435. https://doi.org/10.1007/s11738-003-0025-0.
Tang, C.Q., Dong, Y.F., Herrando-Moraira, S., et al., 2017. Potential effects of climate change on geographic distribution of the Tertiary relict tree species Davidia involucrata in China. Sci. Rep. 7. https://doi.org/10.1038/srep43822.
Wahid, A., Gelani, S., Ashraf, M., et al., 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 62, 199-223. https://doi.org/10.1016/j.envexpbot.2007.05.011.
Weitbrecht, K., Mü Ller, K., Leubner-Metzger, G., 2011. First off the mark: early seed germination. J. Exp. Bot. 62, 3289-3309. https://doi.org/10.1093/jxb/err030.
Yang, Y.G., Lv, W.T., Li, M.J., et al., 2013. Maize membrane-bound transcription factor zmbzip17 is a key regulator in the cross-talk of er quality control and aba signaling. Plant Cell Physiol. 54, 2020-2033. https://doi.org/10.1093/pcp/pct142.
Young, M.D., Wakefield, M.J., Smyth, G.K., et al., 2010. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 11. https://doi.org/10.1186/gb-2010-11-2-r14.
Zhang, J., L, J., Z, B., et al., 1995. Research on the protection of Davidia involucrata populations, a rare and endangered plant endemic to China. J. Beijing For. Univ. 17, 25-30.
Zhao, J., Li, W., Sun, S., et al., 2021. The rice small auxin-up rna gene ossaur33 regulates seed vigor via sugar pathway during early seed germination. Int. J. Mol. Sci. 22, 1-17. https://doi.org/10.3390/ijms22041562.
Zheng, X., Hayashibe, E., Ashihara, H., 2005. Changes in trigonelline (N-methylnicotinic acid) content and nicotinic acid metabolism during germination of mungbean (Phaseolus aureus) seeds. J. Exp. Bot. 56, 1615-1623. https://doi.org/10.1093/JXB/ERI156.

[1]	Yu-Wen Zhang, Yu-Cen Shi, Shi-Bao Zhang. Metabolic and transcriptomic analyses elucidate a novel insight into the network for biosynthesis of carbohydrate and secondary metabolites in the stems of a medicinal orchid Dendrobium nobile[J]. Plant Diversity, 2023, 45(03): 326-336.
[2]	Liang Lin, Lei Cai, Lei Fan, Jun-Chao Ma, Xiang-Yun Yang, Xiao-Jian Hu. Seed dormancy, germination and storage behavior of Magnolia sinica, a plant species with extremely small populations of Magnoliaceae[J]. Plant Diversity, 2022, 44(01): 94-100.
[3]	Li-E Yang, De-Li Peng, Zhi-Min Li, Li Huang, Juan Yang, Hang Sun. Cold stratification, temperature, light, GA₃, and KNO₃ effects on seed germination of Primula beesiana from Yunnan, China[J]. Plant Diversity, 2020, 42(03): 168-173.
[4]	Uma Shankar. Phytosociology of stratification in a lowland tropical rainforest occurring north of the Tropic of Cancer in Meghalaya, India[J]. Plant Diversity, 2019, 41(05): 285-299.
[5]	Jianfang He, Ping Li, Heqiang Huo, Lina Liu, Ting Tang, Mingxia He, Junchao Huang, Li Liu. Heterologous expression of HpBHY and CrBKT increases heat tolerance in Physcomitrella patens[J]. Plant Diversity, 2019, 41(04): 266-274.
[6]	Deli Peng, Zhe Chen, Xiaojian Hu, Zhimin Li, Bo Song, Hang Sun. Seed dormancy and germination characteristics of two Rheum species in the Himalaya-Hengduan Mountains[J]. Plant Diversity, 2017, 39(04): 180-186.
[7]	BASKIN Carol C1 , 2 , BASKIN Jerry M1 . Advances in Understanding Seed Dormancy at the Whole-seed Level: An Ecological , Biogeographical and Phylogenetic Perspective[J]. Plant Diversity, 2008, 30(03): 279-294.

Metabolome profiling of stratified seeds provides insight into the regulation of dormancy in Davidia involucrata

Metabolome profiling of stratified seeds provides insight into the regulation of dormancy in Davidia involucrata

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 7

编辑推荐

Metrics

本文评价