Transcriptomic analysis reveals transcription factors involved in vascular bundle development and tissue maturation in ginger rhizomes (Zingiber officinale Roscoe)
DOI:
https://doi.org/10.15835/nbha51213131Keywords:
ginger, rhizome maturation, transcription factor, transcriptomic analysis, vascular bundle developmentAbstract
Ginger (Zingiber officinale Roscoe) is an important vegetable with medicinal value. Rhizome development determines ginger yield and quality. However, little information is available about the molecular features underlying rhizome expansion and maturation. In this study, we investigated anatomy characteristics, lignin accumulation and transcriptome profiles during rhizome development. In young rhizomes, the vascular bundle (VB) was generated with only vessels in it, whereas in matured rhizomes, three to five layers of fibre bundle in the xylem were formed, resulting in VB enlargement. It indicates VB development favouring rhizome swelling. With rhizome matured, the lignin content was remarkably elevated, thus facilitating tissue lignification. To explore the regulators for rhizome development, nine libraries including ginger young rhizomes (GYR), growing rhizomes (GGR), and matured rhizomes (GMR) were established for RNA-Seq, a total of 1264 transcription factors (TFs) were identified. Among them, 35, 116, and 14 differentially expressed TFs were obtained between GYR and GGR, GYR and GMR, and GGR and GMR, respectively. These TFs were further divided into three categories. Among them, three ZobHLHs (homologs of Arabidopsis LHW and AtbHLH096) as well as one DIVARICATA homolog in ginger might play crucial roles in controlling VB development. Four ZoWRKYs and two ZoNACs might be potential regulators associated with rhizome maturation. Three ZoAP2/ERFs and one ZoARF might participate in rhizome development via hormone signalling. This result provides a molecular basis for rhizome expansion and maturation in ginger.
References
Abogadallah GM, Nada RM, Malinowski R, Quick P (2011). Overexpression of HARDY, an AP2/ERF gene from Arabidopsis, improves drought and salt tolerance by reducing transpiration and sodium uptake in transgenic Trifolium alexandrinum L. Planta 233(6):1265-1276. https://doi.org/10.1007/s00425-011-1382-3
Berleth T, Mattsson J, Hardtke CS (2000). Vascular continuity and auxin signals. Trends in Plant Science 5(9):387-393. https://doi.org/10.1016/S1360-1385(00)01725-8
Breitel DA, Chappell-Maor L, Meir S, Panizel I, Puig CP, Hao Y, . . . Bouzayen M (2016). AUXIN RESPONSE FACTOR 2 intersects hormonal signals in the regulation of tomato fruit ripening. PLoS Genetics 12(3):e1005903. https://doi.org/10.1371/journal.pgen.1005903
Chandler J, Werr W (2020). A phylogenetically conserved APETALA2/ethylene response factor, ERF12, regulates arabidopsis floral development. Plant Molecular Biology 102(1):39-54. https://doi.org/10.1007/s11103-019-00936-5
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a). TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13(8):1194-1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen Z, Tang N, Li H, Liu G, Tang L (2020b). Genome-wide transcriptomic analysis during rhizome development of ginger (Zingiber officinale Roscoe.) reveals hormone and transcriptional regulation involved in cellulose production. Scientia Horticulturae 264:109154. https://doi.org/10.1016/j.scienta.2019.109154
Cheng S-P, Jia K-H, Liu H, Zhang R-G, Li Z-C, Zhou S-S, . . . Gao C (2021). Haplotype-resolved genome assembly and allele-specific gene expression in cultivated ginger. Horticulture Research 8:188. https://doi.org/10.1038/s41438-021-00599-8
Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, . . . Giovannoni J (2010). A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. The Plant journal 64(6):936-947. https://doi.org/10.1111/j.1365-313X.2010.04384.x
De Rybel B, Möller B, Yoshida S, Grabowicz I, de Reuille PB, Boeren S, . . . Weijers D (2013). A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Developmental Cell 24(4):426-437. https://doi.org/10.1016/j.devcel.2012.12.013
Etchells JP, Provost CM, Turner SR (2012). Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLoS Genetics 8(11):e1002997. https://doi.org/10.1371/journal.pgen.1002997
Gan Z, Yuan X, Shan N, Wan C, Chen C, Xu Y, . . . Chen J (2021). AcWRKY40 mediates ethylene biosynthesis during postharvest ripening in kiwifruit. Plant science 309:110948. https://doi.org/10.1016/j.plantsci.2021.110948
Gao G, Zhong Y, Guo A, Zhu Q, Tang W, Zheng W, . . . Luo J (2006). DRTF: a database of rice transcription factors. Bioinformatics 22(10):1286-1287. https://doi.org/10.1093/bioinformatics/btl107
Gao J, Zhang Y, Li Z, Liu M (2020). Role of ethylene response factors (ERFs) in fruit ripening. Food Quality and Safety 4(1):15-20. https://doi.org/10.1093/fqsafe/fyz042
Gao Y, Wei W, Zhao X, Tan X, Fan Z, Zhang Y, . . . Zhu H (2018). A NAC transcription factor, NOR-like1, is a new positive regulator of tomato fruit ripening. Horticulture Research 5:75. https://doi.org/10.1038/s41438-018-0111-5
Godiard L, Lepage A, Moreau S, Laporte D, Verdenaud M, Timmers T, Gamas P (2011). MtbHLH1, a bHLH transcription factor involved in Medicago truncatula nodule vascular patterning and nodule to plant metabolic exchanges. New Phytologist 191(2):391-404. https://doi.org/10.1111/j.1469-8137.2011.03718.x
Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005). DATF: a database of Arabidopsis transcription factors. Bioinformatics 21(10):2568-2569. https://doi.org/10.1093/bioinformatics/bti334
Guo L, Plunkert M, Luo X, Liu Z (2021). Developmental regulation of stolon and rhizome. Current Opinion in Plant Biology 59:101970. https://doi.org/10.1016/j.pbi.2020.10.003
Hong Y, Zhang H, Huang L, Li D, Song F (2016). Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. Frontiers in Plant Science 7:4. https://doi.org/10.3389/fpls.2016.0000
Hu F, Wang D, Zhao X, Zhang T, Sun H, Zhu L, . . . Tao D (2011). Identification of rhizome-specific genes by genome-wide differential expression analysis in Oryza longistaminata. BMC Plant Biology 11(1):1-14. https://doi.org/10.1186/1471-2229-11-18
Hu Q, Xiao S, Wang X, Ao C, Zhang X, Zhu L (2021). GhWRKY1-like enhances cotton resistance to Verticillium dahliae via an increase in defense-induced lignification and S monolignol content. Plant science 305:110833. https://doi.org/10.1016/j.plantsci.2021.110833
Hu R, Yu C, Wang X, Jia C, Pei S, He K, . . . Zhou G (2017). De novo transcriptome analysis of Miscanthus lutarioriparius identifies candidate genes in rhizome development. Frontiers in Plant Science 8:492. https://doi.org/10.3389/fpls.2017.00492
Hughes TE, Sedelnikova OV, Wu H, Becraft PW, Langdale JA (2019). Redundant SCARECROW genes pattern distinct cell layers in roots and leaves of maize. Development 146(14):dev177543. https://doi.org/10.1242/dev.177543
Jiang Y, Huang M, Wisniewski M, Li H, Zhang M, Tao X, Liu Y, Zou Y (2018a). Transcriptome analysis provides insights into gingerol biosynthesis in ginger (Zingiber officinale). The Plant Genome 11(3):180034. https://doi.org/10.3835/plantgenome2018.06.0034
Jiang Y, Huang M, Zhang M, Lan J, Wang W, Tao X, Liu Y (2018b). Transcriptome analysis provides novel insights into high-soil-moisture-elevated susceptibility to Ralstonia solanacearum infection in ginger (Zingiber officinale Roscoe cv. Southwest). Plant Physiology and Biochemistry 132:547-556. https://doi.org/10.1016/j.plaphy.2018.10.005
Katayama H, Iwamoto K, Kariya Y, Asakawa T, Kan T, Fukuda H, Ohashi-Ito K (2015). A negative feedback loop controlling bHLH complexes is involved in vascular cell division and differentiation in the root apical meristem. Current Biology 25(23):3144-3150. https://doi.org/10.1016/j.cub.2015.10.051
Kim JH, Lee BH (2006). Growth-regulating FACTOR4 ofArabidopsis thaliana is required for development of leaves, cotyledons, and shoot apical meristem. Journal of Plant Biology 49(6):463-468. https://doi.org/10.1007/BF03031127
Koo H, McDowell ET, Ma X, Greer KA, Kapteyn J, Xie Z, . . . Kudrna D (2013). Ginger and turmeric expressed sequence tags identify signature genes for rhizome identity and development and the biosynthesis of curcuminoids, gingerols and terpenoids. BMC Plant Biology 13(1):1-17. https://doi.org/10.1186/1471-2229-13-27
Li H-L, Wu L, Dong Z, Jiang Y, Jiang S, Xing H, . . . Wu Z (2021). Haplotype-resolved genome of diploid ginger (Zingiber officinale) and its unique gingerol biosynthetic pathway. Horticulture Research 8:189. https://doi.org/10.1038/s41438-021-00627-7
Li H, Wu L, Tang N, Liu R, Jin Z, Liu Y, Li Z (2020). Analysis of transcriptome and phytohormone profiles reveal novel insight into ginger (Zingiber officinale Rose) in response to postharvest dehydration stress. Postharvest Biology and Technology 161:111087. https://doi.org/10.1016/j.postharvbio.2019.111087
Li X, Chen T, Li Y, Wang Z, Cao H, Chen F, . . . Liu Y (2019). ETR1/RDO3 regulates seed dormancy by relieving the inhibitory effect of the ERF12-TPL complex on DELAY OF GERMINATION1 expression. The Plant Cell 31(4):832-847. https://doi.org/10.1105/tpc.18.00449
Li Z-Y, Li B, Dong A-W (2012). The Arabidopsis transcription factor AtTCP15 regulates endoreduplication by modulating expression of key cell-cycle genes. Molecular Plant 5(1):270-280. https://doi.org/10.1093/mp/ssr086
Liang S-m, Chen S-c, Liu Z-l, Shan W, Chen J-y, Lu W-j, Lakshmanan P, Kuang J-f (2020). MabZIP74 interacts with MaMAPK11-3 to regulate the transcription of MaACO1/4 during banana fruit ripening. Postharvest Biology and Technology 169:111293. https://doi.org/10.1016/j.postharvbio.2020.111293
Liu G-S, Li H-L, Grierson D, Fu D-Q (2022). NAC transcription factor family regulation of fruit ripening and quality: A Review. Cells 11(3):525. https://doi.org/10.3390/cells11030525
Liu H, Specht CD, Zhao T, Liao J (2020). Morphological anatomy of leaf and rhizome in Zingiber officinale Roscoe, with emphasis on secretory structures. HortScience 55(2):204-207. https://doi.org/10.21273/HORTSCI14555-19
Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei Z, . . . Van Der Knaap E (2014). Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. Journal of Experimental Botany 65(9):2507-2520. https://doi.org/10.1093/jxb/eru141
Liu Y, Shi Y, Su D, Lu W, Li Z (2021). SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato. Horticulture Research 8:3. https://doi.org/10.1038/s41438-020-00431-9
Love MI, Huber W, Anders S (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15(12):1-21. https://doi.org/10.1186/s13059-014-0550-8
Ma X, Xu Q, Meyer WA, Huang B (2016). Hormone regulation of rhizome development in tall fescue (Festuca arundinacea) associated with proteomic changes controlling respiratory and amino acid metabolism. Annals of Botany 118(3):481-494. https://doi.org/10.1093/aob/mcw120
Machemer K, Shaiman O, Salts Y, Shabtai S, Sobolev I, Belausov E, . . . Barg R (2011). Interplay of MYB factors in differential cell expansion, and consequences for tomato fruit development. The Plant Journal 68(2):337-350. https://doi.org/10.1111/j.1365-313X.2011.04690.x
Ohtani M, Demura T (2019). The quest for transcriptional hubs of lignin biosynthesis: beyond the NAC-MYB-gene regulatory network model. Current Opinion in Biotechnology 56:82-87. https://doi.org/10.1016/j.copbio.2018.10.002
Prasath D, Karthika R, Habeeba NT, Suraby EJ, Rosana OB, Shaji A, . . . Anandaraj M (2014). Comparison of the transcriptomes of ginger (Zingiber officinale Rosc.) and mango ginger (Curcuma amada Roxb.) in response to the bacterial wilt infection. PLoS ONE 9(6):e99731. https://doi.org/10.1371/journal.pone.0099731
Rayirath UP, Lada RR, Caldwell CD, Asiedu SK, Sibley KJ (2011). Role of ethylene and jasmonic acid on rhizome induction and growth in rhubarb (Rheum rhabarbarum L.). Plant Cell, Tissue and Organ Culture (PCTOC) 105(2):253-263. https://doi.org/10.1007/s11240-010-9861-y
Schulze SK, Kanwar R, Gölzenleuchter M, Therneau TM, Beutler AS (2012). SERE: single-parameter quality control and sample comparison for RNA-Seq. BMC Genomics 13(1):1-9. https://doi.org/10.1186/1471-2164-13-524
Silveira AB, Gauer L, Tomaz JP, Cardoso PR, Carmello-Guerreiro S, Vincentz M (2007). The Arabidopsis AtbZIP9 protein fused to the VP16 transcriptional activation domain alters leaf and vascular development. Plant Science 172(6):1148-1156. https://doi.org/10.1016/j.plantsci.2007.03.003
Sun Y, Jiang C, Jiang R, Wang F, Zhang Z, Zeng J (2021). A novel NAC transcription factor from Eucalyptus, EgNAC141, positively regulates lignin biosynthesis and increases lignin deposition. Frontiers in Plant Science 12:642090. https://doi.org/10.3389/fpls.2021.642090
Teng R, Wang Y, Lin S, Chen Y, Yang Y, Yang N, . . . Zhuang J (2021). CsWRKY13, a novel WRKY transcription factor of Camellia sinensis, involved in lignin biosynthesis and accumulation. Beverage Plant Research 1(1):1-9. https://doi.org/10.48130/BPR-2021-0012
Vera-Sirera F, De Rybel B, Urbez C, Kouklas E, Pesquera M, Alvarez-Mahecha JC, . . . Borst JW (2015). A bHLH-based feedback loop restricts vascular cell proliferation in plants. Developmental Cell 35(4):432-443. https://doi.org/10.1016/j.devcel.2015.10.022
Wang K, Peng H, Lin E, Jin Q, Hua X, Yao S, . . . Wang J (2010). Identification of genes related to the development of bamboo rhizome bud. Journal of Experimental Botany 61 (2):551-561. https://doi.org/10.1093/jxb/erp334
Wang T, Yang Y, Lou S, Wei W, Zhao Z, Ren Y, . . . Ma L (2019). Genome-wide characterization and gene expression analyses of GATA transcription factors in Moso bamboo (Phyllostachys edulis). International Journal of Molecular Sciences 21(1):14. https://doi.org/10.3390/ijms21010014
Wen W, Wang R, Su L, Lv A, Zhou P, An Y (2021). MsWRKY11, activated by MsWRKY22, functions in drought tolerance and modulates lignin biosynthesis in alfalfa (Medicago sativa L.). Environmental and Experimental Botany 184:104373. https://doi.org/10.1016/j.envexpbot.2021.104373
Xing H, Jiang Y, Zou Y, Long X, Wu X, Ren Y, . . . Li H-L (2021). Genome-wide investigation of the AP2/ERF gene family in ginger: evolution and expression profiling during development and abiotic stresses. BMC Plant Biology 21(1):1-21. https://doi.org/10.1186/s12870-021-03329-3
Xu B, Sathitsuksanoh N, Tang Y, Udvardi MK, Zhang J-Y, Shen Z, . . . Zhao B (2012). Overexpression of AtLOV1 in switchgrass alters plant architecture, lignin content, and flowering time. PLoS ONE 7(12):e47399. https://doi.org/10.1371/journal.pone.0047399
Xu C, Shen Y, He F, Fu X, Yu H, Lu W, . . . Wang HC (2019). Auxin‐mediated Aux/IAA‐ARF‐HB signaling cascade regulates secondary xylem development in Populus. New Phytologist 222(2):752-767. https://doi.org/10.1111/nph.15658
Xu Q, Wang W, Zeng J, Zhang J, Grierson D, Li X, . . . Chen K (2015). A NAC transcription factor, EjNAC1, affects lignification of loquat fruit by regulating lignin. Postharvest Biology and Technology 102:25-31. https://doi.org/10.1016/j.postharvbio.2015.02.002
Yamagishi K, Tatematsu K, Yano R, Preston J, Kitamura S, Takahashi H, . . . Nambara E (2009). CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant and Cell Physiology 50(2):330-340. https://doi.org/10.1093/pcp/pcn201
Yan H, Jiang G, Wu F, Li Z, Xiao L, Jiang Y, Duan X (2021). Sulfoxidation regulation of transcription factor NAC42 influences its functions in relation to stress-induced fruit ripening in banana. Journal of Experimental Botany 72(2):682-699. https://doi.org/10.1093/jxb/eraa474
Yang M, Zhu L, Pan C, Xu L, Liu Y, Ke W, Yang P (2015). Transcriptomic analysis of the regulation of rhizome formation in temperate and tropical lotus (Nelumbo nucifera). Scientific Reports 5(1):1-17. https://doi.org/10.1038/srep13059
Yang W, Liu W, Niu K, Ma X, Jia Z, Ma H, . . . Liu M (2022). Transcriptional regulation of different rhizome parts reveal the candidate genes that regulate rhizome development in Poa pratensis. DNA and Cell Biology 41(2):151-168. https://doi.org/10.1089/dna.2021.0337
Yu Y, Qi Y, Xu J, Dai X, Chen J, Dong CH, Xiang F (2021). Arabidopsis WRKY71 regulates ethylene‐mediated leaf senescence by directly activating EIN2, ORE1 and ACS2 genes. The Plant Journal 107(6):1819-1836. https://doi.org/10.1111/tpj.15433
Zhang S, Wang L, Sun X, Li Y, Yao J, Nocker Sv, Wang X (2019). Genome-wide analysis of the YABBY gene family in grapevine and functional characterization of VvYABBY4. Frontiers in Plant Science 10:1207. https://doi.org/10.3389/fpls.2019.01207
Zhang X, Ran D, Wu P, Cao Z, Xu F, Xia N, . . . He N (2022). Transcriptome and metabolite profiling to identify genes associated with rhizome lignification and the function of ZoCSE in ginger (Zingiber officinale). Functional Plant Biology 49(8):689-703. https://doi.org/10.1071/FP21267
Zheng S, He J, Lin Z, Zhu Y, Sun J, Li L (2021). Two MADS-box genes regulate vascular cambium activity and secondary growth by modulating auxin homeostasis in Populus. Plant Communications 2(5):100134. https://doi.org/10.1016/j.xplc.2020.100134
Zhong R, Ye Z-H (2004). Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant and Cell Physiology 45(4):369-385. https://doi.org/10.1093/pcp/pch051
Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Li W, Zhang H (2010). The Arabidopsis AP2/ERF transcription factor RAP2. 6 participates in ABA, salt and osmotic stress responses. Gene 457(1-2):1-12. https://doi.org/10.1016/j.gene.2010.02.011
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Zhengyan CAO, Ning TANG, Zexiong CHEN, Peiyin WU, Jiarui ZHENG, Jiabao YE, Yanni LIU, Yang HU, Li ZHANG, Xiaofan SUN, Zhenqi LIU, Feng XU
This work is licensed under a Creative Commons Attribution 4.0 International License.
License:
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.