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Journal of Integrative Agriculture
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Transcriptome-based analysis of lignin accumulation in the regulation of fruit stone development and endocarp hardening in Chinese jujube

Xinyi Mao1*, Xuan Zhao1, 2*, Zhi Luo1*, Ao He1*, Meng Yang1, Mengjun Liu1, 2, Jin Zhao3#, Ping Liu1, 2#

1 College of Horticulture, Hebei Agricultural University, Baoding Hebei 071001, China

2 Research Center of Chinese Jujube, Hebei Agricultural University, Baoding Hebei 071001, China

3 College of Life Science, Hebei Agricultural University, Baoding, 071000 China

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摘要  

核果进化出一种极其坚硬的木质外壳,称为果核,用以保护种子。如今,无核栽培品种的市场价值急剧上升,这就提出了培育无核果实的需求。因此,迫切需要了解果核的内在机理。我们利用中国枣的一个有核栽培品种有核和两个无核栽培品种无核大果无核,对枣果核发育机理进行了全面研究。通过解剖分析和木质素染色检测发现,有核栽培品种有核的内果皮木质素积累量远高于其他两个无核栽培品种。木质素积累可能是形成果核的关键原因。通过分析转录组数据并识别其中的差异表达基因(DEGs),发现有核无核丰以及有核大果无核之间有49个重叠的DEGs。其中,参与木质素合成的ZjF6H1-3ZjPOD被鉴定出来。在野生酸枣幼苗上过表达和沉默ZjF6H1-3ZjPOD进一步验证了它们在木质素合成中的作用。此外,在这49个重叠的DEGs中还包括两个bHLH转录因子,并且在ZjF6H1-3ZjPOD的启动子中发现了bHLH转录因子基序,这表明bHLH转录因子也参与了木质素的合成。



Abstract  

Stone fruits, also known as drupes, have evolved an extremely hard wood-like shell called a stone to protect seeds. Currently, the market value of stoneless cultivars has risen dramatically, which highlights the need to cultivate stoneless fruit. Therefore, the underlying mechanism of fruit stones is urgently needed. By employing the stone-containing jujube cultivar ‘Youhe’ and two stoneless Chinese jujube cultivars, ‘Wuhefeng’ and ‘Jinsixiaozao’, we carried out a comprehensive study on the mechanism of fruit stone development in jujube. Anatomical analysis and lignin staining revealed that the stone cultivar ‘Youhe’ jujube exhibited much greater lignin accumulation in the endocarp than did the other two stoneless cultivars. Lignin accumulation may be the key reason for the formation of fruit stone. By analysing the transcriptome data and identifying differentially expressed genes (DEGs), 49 overlapping DEGs between ‘Youhe’ jujube vs ‘Wuhefeng’ jujube and ‘Youhe’ jujube vs ‘Daguowuhe’ jujube were identified. Among these DEGs, ZjF6H1-3 and ZjPOD, which are involved in lignin synthesis, were identified. Overexpression and silencing of ZjF6H1-3 and ZjPOD in wild jujube seedlings further confirmed their role in lignin synthesis. In addition, two bHLH transcription factors were also included in these 49 overlapping DEGs, and bHLH transcription factor motifs were found in the promoters of ZjF6H1-3 and ZjPOD, indicating that bHLH transcription factors are also involved in lignin synthesis and stone formation in Chinese jujube. This study provides new insight into the molecular networks underlying fruit stone formation and provides an important reference for the molecular design and breeding of stoneless fruit cultivars for jujube and fruit trees.

Keywords:  Chinese jujube       fruit stone              lignin              endocarp              phenylpropanoid pathway              transcriptome analysis  
Online: 31 December 2024  
Fund: 

This research was supported by the Central Fund for Promoting Innovative Technology Development (236Z6801G), Hebei Provincial Modern Seed Industry Technology Innovation Team-Dried Fruits (21326304D), Construction of Innovative Teams for the Modern Agricultural Industry System in Hebei Province (HBCT2023120210, HBCT2024190203).

About author:  #Correspondence Jin Zhao, E-mail zhaojinbd@126.com; Ping Liu, E-mail: yylp@hebau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Xinyi Mao, Xuan Zhao, Zhi Luo, Ao He, Meng Yang, Mengjun Liu, Jin Zhao, Ping Liu. 2024. Transcriptome-based analysis of lignin accumulation in the regulation of fruit stone development and endocarp hardening in Chinese jujube. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.12.032

Bu J, Zhao J, Liu M. 2016. Expression stabilities of candidate reference genes for RT-qPCR in Chinese Jujube (Ziziphus jujuba Mill.) under a variety of conditions. PLOS ONE. doi,10.1371/journal.pone.0154212.

Dai H, Han G, Yan Y, Zhang F, Liu Z, Li X, Li W, Ma Y, Li H, Liu Y, Zhang Z. 2013. Transcript assembly and quantification by RNA-Seq reveals differentially expressed genes between soft-endocarp and hard-endocarp Hawthorns. PLOS ONE, 8, e72910. doi,10.1371/journal.pone.0072910.

Dardick C, Callahan A M. 2014a. Evolution of the fruit endocarp: molecular mechanisms underlying adaptations in seed protection and dispersal strategies. Frontiers in Plant Science, 5, 284. doi,10.3389/fpls.2014.00284.

Dardick C, Callahan A M. 2014b. Evolution of the fruit endocarp: molecular mechanisms underlying adaptations in seed protection and dispersal strategies. Frontiers in Plant Science, 5, 285. doi,10.3389/fpls.2014.00284.

Dardick C D, Callahan A M, Chiozzotto R, Schaffer R J, Piagnani M C, Scorza R. 2010. Stone formation in peach fruit exhibits spatial coordination of the lignin and flavonoid pathways and similarity to Arabidopsis dehiscence. BMC Biology, 8, 1-17. doi,10.1186/1741-7007-8-13.

Gao Q-H, Wu C-S, Wang M. 2013. The Jujube (Ziziphus Jujuba Mill.) Fruit: A review of current knowledge of fruit composition and health benefits. Journal of Agricultural and Food Chemistry, 61, 3351-3363. doi,10.1021/jf4007032.

Gao Z, Sun W, Wang J, Zhao C, Zuo K. 2019. GhbHLH18 negatively regulates fiber strength and length by enhancing lignin biosynthesis in cotton fibers. Plant Science, 286, 7-16. doi,10.1016/j.plantsci.2019.05.020.

Gui J, Shen J, Li L. 2011. Functional characterization of evolutionarily divergent 4-coumarate:coenzyme a ligases in Rice. Plant Physiology. doi,10.1104/pp.111.178301.

Hu S, Kamimura N, Sakamoto S, Nagano S, Takata N, Liu S, Goeminne G, Vanholme R, Uesugi M, Yamamoto M, Hishiyama S, Kim H, Boerjan W, Ralph J, Masai E, Mitsuda N, Kajita S. 2022. Rerouting of the lignin biosynthetic pathway by inhibition of cytosolic shikimate recycling in transgenic hybrid aspen. The Plant Journal. doi,10.1111/tpj.15674.

Jin Q, Yan C, Qiu J, Zhang N, Lin Y, Cai Y. 2013. Structural characterization and deposition of stone cell lignin in Dangshan Su pear. Scientia Horticulturae, 155, 123-130. doi,10.1016/j.scienta.2013.03.020.

Keli Q, Hui Z, Haifa P, Yu S, Hong Y, Qingmei X, Hongli C, Yongping C, Jinyun Z, Jinling H. 2022. Genome-wide identification and functional analysis of the peach (P. persica) laccase gene family reveal members potentially involved in endocarp lignification. Trees. doi,10.1007/s00468-022-02296-y.

Khan M K U, Muhammad N, Jia Z, Peng J, Liu M. 2022a. Mechanism of stone (hardened endocarp) formation in fruits: an attempt toward pitless fruits, and its advantages and disadvantages. Genes. doi,10.3390/genes13112123.

Khan M K U, Muhammad N, Jia Z, Peng J, Liu M. 2022b. Mechanism of stone (hardened endocarp) formation in fruits: an attempt toward pitless Fruits, and Its advantages and disadvantages. Genes, 13 2123. doi,10.3390/genes13112123.

Lam C T W, Chan P H, Lee P S C, Lau K M, Kong A Y Y, Gong A G W, Xu M L, Lam K Y C, Dong T T X, Lin H, Tsim K W K. 2015. Chemical and biological assessment of Jujube (Ziziphus jujuba)-containing herbal decoctions: Induction of erythropoietin expression in cultures. Journal of Chromatography B, 1026, 254-262. doi,10.1016/j.jchromb.2015.09.021.

Lam C T W, Gong A G W, Lam K Y C, Zhang L M, Chen J-P, Dong T T X, Lin H-Q, Tsim K W K. 2016. Jujube-containing herbal decoctions induce neuronal differentiation and the expression of anti-oxidant enzymes in cultured PC12 cells. Journal of Ethnopharmacology, 188, 275-283. doi,10.1016/j.jep.2016.05.015.

Lee C-J, Park S-U, Kim S-E, Lim Y-H, Ji C Y, Kim Y-H, Kim H S, Kwak S-S. 2021. Overexpression of IbLfp in sweetpotato enhances the low-temperature storage ability of tuberous roots. Plant Physiology and Biochemistry, 167, 577-585. doi,10.1016/j.plaphy.2021.08.041.

Li H, Shengjie D, Wenna Z, Zhenning L, Yuli S, Yaqin Z, Meng X. 2023. Transcriptome analysis of walnut (Juglans regia L.) fruit reveals the function of JrMYB180 in GA3-induced endocarp lignification. Plant Growth Regulation, 1-9. doi,10.1007/s10725-023-00963-9.

Li W, Amos K, Li M, Pu Y, Debolt S, Ragauskas A J, Shi J. 2018. Fractionation and characterization of lignin streams from unique high-lignin content endocarp feedstocks. Biotechnology for Biofuels, 11, 1-14. doi,10.1186/s13068-018-1305-7.

Livak K J, Schmittgen T D. 2002. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25, 402-408. doi,10.1006/meth.2001.1262.

Long X. 2000. Modern Chinese fruit cultivation, deciduous fruit trees volume. China Forestry Publishing House, Beijing, China, pp. pp. 239-268.

Ma Z, Jia Y. 1991. The causes of seedless fruit and the way to produce it. Journal of Biology, 5-7+4.

Meng Z, Jia Y, Aizhen Y, Guanglu S, Tieqiang Z, Younian W. 2016. The lignin deposition process in fruit endocarp of different Jujube cultivars. Journal of Agriculture, 6, 82-87.

Niu N, Zhang Y, Li S, Meng X, Liu M, Wang H, Zhao J. 2023. Genome-wide characterization of the cellulose synthase gene family in Ziziphus jujuba reveals its function in cellulose biosynthesis during fruit development. International Journal of Biological Macromolecules, 239, 124360. doi,10.1016/j.ijbiomac.2023.124360.

Qu Z, Wang Y H. 1993. Chinese Fruit Tree Chronicle Jujube Roll. China Forestry Press, BeiJing. 498.

Qui K, Zhou H, Pan H, Sheng Y, Yu H, Xie Q, Chen H, Cai Y, Zhang J, He J. 2022. Genome-wide identification and functional analysis of the peach (P. persica) laccase gene family reveal members potentially involved in endocarp lignification. Trees, 36, 1477-1496. doi,10.1007/s00468-022-02296-y.

Rencoret J, Kim H, Evaristo A B, Gutiérrez A, Ralph J, del Río J C. 2017. Variability in lignin composition and structure in cell walls of different parts of Macaúba (Acrocomia aculeata) Palm fruit. Journal of Agricultural and Food Chemistry, 66, 138-153. doi,10.1021/acs.jafc.7b04638.

Sakamoto S, Kamimura N, Tokue Y, Nakata M T, Yamamoto M, Hu S, Masai E, Mitsuda N, Kajita S. 2020. Identification of enzymatic genes with the potential to reduce biomass recalcitrance through lignin manipulation in Arabidopsis. Biotechnology for Biofuels, 13, 1-16. doi,10.1186/s13068-020-01736-6.

Schmid N B, Giehl R F H, Döll S, Mock H-P, Strehmel N, Scheel D, Kong X, Hider R C, von Wirén N. 2013. Feruloyl-CoA 6'-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiology, 164, 160-172. doi,10.1104/pp.113.228544.

Shi J, Yan X, Sun T, Shen Y, Shi Q, Wang W, Bao M, Luo H, Nian F, Ning G. 2021. Homeostatic regulation of flavonoid and lignin biosynthesis in phenylpropanoid pathway of transgenic tobacco. Gene, 809, 146017. doi,10.1016/j.gene.2021.146017.

Tan H H. 2013. lsolation and expression of two genes related to lignin synthesis in Chinese jujube fruit. Nanjing Agricultural University, Nanjing.

Teichman I V, Van Wyk A E. 1993. Ontogeny and structure of the drupe of Ozoroa paniculosa (Anacardiaceae). Botanical Journal of the Linnean Society. doi,10.1111/j.1095-8339.1993.tb01902.x.

Wang H B, Zhu J, Wang D Y. 2013. Analysis of the content of pear pulp stone cells.,Jiangsu Journal of Agricultural, 46, 173-176.

Xue Y, Shan Y, Yao J-L, Wang R, Xu S, Liu D, Ye Z, Lin J, Li X, Xue C, Wu J. 2023. The transcription factor PbrMYB24 regulates lignin and cellulose biosynthesis in stone cells of pear fruits. Plant Physiology. doi,10.1093/plphys/kiad200.

Yan L, Xu C, Kang Y, Gu T, Wang D, Zhao S, Xia G. 2013. The heterologous expression in Arabidopsis thaliana of sorghum transcription factor SbbHLH1 downregulates lignin synthesis. Journal of Experimental Botany, 64, 3021-3032. doi,10.1093/jxb/ert150.

Yao T, Feng K, Xie M, Barros J, Tschaplinski T J, Tuskan G A, Muchero W, Chen J-G. 2021. Phylogenetic occurrence of the phenylpropanoid pathway and lignin biosynthesis in plants. Frontiers in Plant Science, 12, 704697. doi,10.3389/fpls.2021.704697.

Zhang X, Zhang L, Zhang Q, Xu J, Liu W, Dong W. 2017. Comparative transcriptome profiling and morphology provide insights into endocarp cleaving of apricot cultivar (Prunus armeniaca L.). BMC Plant Biology, 17, 1-14. doi,10.1186/s12870-017-1023-5.

Zhao S, Wen J, Wang H, Zhang Z, Li X. 2016. Changes in lignin content and activity of related enzymes in the endocarp during the walnut shell development period. Horticultural Plant Journal, 2, 141-146. doi,10.1016/j.hpj.2016.08.003.

Zhao W, Ding L, Liu J, Zhang X, Li S, Zhao K, Guan Y, Song A, Wang H, Chen S, Jiang J, Chen F. 2022. Regulation of lignin biosynthesis by an atypical bHLH protein CmHLB in Chrysanthemum. Journal of Experimental Botany, 73, 2403-2419. doi,10.1093/jxb/erac015.

Zhao X, Jiang X, Li Z, Song Q, Xu C, Luo K. 2023. Jasmonic acid regulates lignin deposition in poplar through JAZ5-MYB/NAC interaction. Frontiers in Plant Science. doi,10.3389/fpls.2023.1232880.

Zhu Z, Wen Y, Zhou Q, Wu F, Du X, Sheng F. 2024. Mechanism of loding residence and drought tolerance of OsCNGC10 gene in rice. ACTA AGRONOMICA SINICA 50, 1351-1360. doi, 10.3724/SP.J.1006.2024.32027 

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