Genome-wide identification, characterization, and expression profiles of auxin responsive GH3 gene family in Salvia miltiorrhiza involved in MeJA treatment

Abstract

GH3 (Gretchen Hagen 3) is a gene family involved in the response to auxin and plays a role in regulation of plant growth, development and stress responses. The GH3 gene family has been well investigated in genome wide in various plants containing Arabidopsis, rice, maize, etc. However, the study on the GH3 family and its roles involved in JA-signal pathway in Salvia miltiorrhiza is lacking. In this study, we performed a systematic identification of the SmGH3 gene family in genome wide and detected 11 members on 8 S. miltiorrhiza scaffolds. Phylogenetic analyses revealed that SmGH3 proteins could be clustered in two major categories with groups 1 and 2 of GH3 family of Arabidopsis. Diversified cis-elements in the promoter of SmGH3 were predicted as essential players in regulating SmGH3 expression patterns by using PlantCARE database. Gene structure and motif analyses indicated that most SmGH3 genes had relatively conserved exon/intron arrangements and motif compositions. RNA-seq analysis and RT-qPCR showed that 3 SmGH3s (SmGH3.2, SmGH3.6, and SmGH3.10) were up-regulated in S. miltiorrhiza treated by MeJA. Moreover, tissue-specific expression patterns of each SmGH3 genes in different tissues suggested that the various members of GH3 genes conducted their role in the different tissues of S. miltiorrhiza. These results would provide a comprehensive understanding of the GH3 gene family in S. miltiorrhiza and lay a foundation for exploration of their functional divergence and genetic manipulation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

GH3:

Gretchen Hagen 3

IAA:

Indole-3-aceticacid

JA:

Jasmonic acid

SA:

Salicylic acid

MeJA:

Methyl jasmonate

ML:

Maximum likelyhood

References

  1. Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17. https://doi.org/10.1104/pp.111.1.9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106. https://doi.org/10.1186/gb-2010-11-10-r106

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Atkinson NJ, Lilley CJ, Urwin PE (2013) Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol 162:2028–2041. https://doi.org/10.1104/pp.113.222372

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucl Acids Res 43:W39–W49. https://doi.org/10.1093/nar/gkv416

    CAS  Article  PubMed  Google Scholar 

  5. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Bottcher C, Boss PK, Davies C (2011) Acyl substrate preferences of an IAA-amido synthetase account for variations in grape (Vitis vinifera L.) berry ripening caused by different auxinic compounds indicating the importance of auxin conjugation in plant development. J Exp Bot 62:4267–4280. https://doi.org/10.1093/jxb/err134

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Chen Y, Hao X, Cao J (2014) Small auxin upregulated RNA (SAUR) gene family in maize: identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghum. J Integr Plant Biol 56:133–150. https://doi.org/10.1111/jipb.12127

    CAS  Article  PubMed  Google Scholar 

  8. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009

    CAS  Article  PubMed  Google Scholar 

  9. Cheng TO (2006) Danshen: a popular Chinese cardiac herbal drug. J Am Coll Cardiol 47:1499–1500. https://doi.org/10.1016/j.jacc.2006.01.001

    Article  Google Scholar 

  10. Coate JE, Doyle JJ (2010) Quantifying whole transcriptome size, a prerequisite for understanding transcriptome evolution across species: an example from a plant allopolyploid. Genome Biol Evol 2:534–546. https://doi.org/10.1093/gbe/evq038

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  12. Feng S, Yue R, Tao S, Yang Y, Zhang L, Xu M, Wang H, Shen C (2015) Genome-wide identification, expression analysis of auxin-responsive GH3 family genes in maize (Zea mays L.) under abiotic stresses. J Integr Plant Biol 57:783–795. https://doi.org/10.1111/jipb.12327

    CAS  Article  PubMed  Google Scholar 

  13. Feng L, Li G, He Z, Han W, Sun J, Huang F, Di J, Chen Y (2019) The ARF, GH3, and Aux/IAA gene families in castor bean (Ricinus communis L.): genome-wide identification and expression profiles in high-stalk and dwarf strains. Ind Crops Prod 141:111804. https://doi.org/10.1016/j.indcrop.2019.111804

    CAS  Article  Google Scholar 

  14. Guilfoyle TJ (1999) Auxin-regulated genes and promoters. In: Hooykaas PJ, Hall MA, Libbenga KR (eds) Biochemistry and molecular biology of plant hormones. New comprehensive biochemistry. Elsevier, Amsterdam, pp 423–459. https://doi.org/10.1016/s0167-7306(08)60499-8

    Google Scholar 

  15. Guilfoyle TJ, Hagen G (2001) Auxin response factors. J Plant Growth Regul 20:281–291. https://doi.org/10.1007/s003440010026

    CAS  Article  Google Scholar 

  16. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    CAS  Article  Google Scholar 

  17. Han L-M, Hua W-P, Cao X-Y, Yan J-A, Chen C, Wang Z-Z (2020) Genome-wide identification and expression analysis of the superoxide dismutase (SOD) gene family in Salvia miltiorrhiza. Gene. https://doi.org/10.1016/j.gene.2020.144603

    Article  PubMed  Google Scholar 

  18. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817

    Article  PubMed  Google Scholar 

  19. Jain M, Kaur N, Tyagi AK, Khurana JP (2006) The auxin-responsive GH3 gene family in rice (Oryza sativa). Funct Integr Genom 6:36–46. https://doi.org/10.1007/s10142-005-0142-5

    CAS  Article  Google Scholar 

  20. Jiang W, Yin J, Zhang H, He Y, Shuai S, Chen S, Cao S, Li W, Ma D, Chen H (2020) Genome-wide identification, characterization analysis and expression profiling of auxin-responsive GH3 family genes in wheat (Triticum aestivum L.). Mol Biol Rep 47:3885–3907. https://doi.org/10.1007/s11033-020-05477-5

    CAS  Article  PubMed  Google Scholar 

  21. Jin JF, Wang ZQ, He QY, Wang JY, Li PF, Xu JM, Zheng SJ, Fan W, Yang JL (2020) Genome-wide identification and expression analysis of the NAC transcription factor family in tomato (Solanum lycopersicum) during aluminum stress. BMC Genom 21:288. https://doi.org/10.1186/s12864-020-6689-7

    CAS  Article  Google Scholar 

  22. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275

    CAS  Article  PubMed  Google Scholar 

  23. Kai G, Xu H, Zhou C, Liao P, Xiao J, Luo X, You L, Zhang L (2011) Metabolic engineering tanshinone biosynthetic pathway in Salvia miltiorrhiza hairy root cultures. Metab Eng 13:319–327. https://doi.org/10.1016/j.ymben.2011.02.003

    CAS  Article  PubMed  Google Scholar 

  24. Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665. https://doi.org/10.1093/aob/mct229

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858. https://doi.org/10.1038/nprot.2015.053

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Kirungu JN, Magwanga RO, Lu P, Cai X, Zhou Z, Wang X, Peng R, Wang K, Liu F (2019) Functional characterization of Gh_A08G1120 (GH3.5) gene reveal their significant role in enhancing drought and salt stress tolerance in cotton. BMC Genet 20:62. https://doi.org/10.1186/s12863-019-0756-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Kong W, Zhong H, Deng X, Gautam M, Gong Z, Zhang Y, Zhao G, Liu C, Li Y (2019) Evolutionary analysis of GH3 genes in six Oryza species/subspecies and their expression under salinity stress in Oryza sativa ssp. japonica. Plants (Basel). https://doi.org/10.3390/plants8020030

    Article  PubMed Central  Google Scholar 

  28. Kumar R, Agarwal P, Tyagi AK, Sharma AK (2012) Genome-wide investigation and expression analysis suggest diverse roles of auxin-responsive GH3 genes during development and response to different stimuli in tomato (Solanum lycopersicum). Mol Genet Genom 287:221–235. https://doi.org/10.1007/s00438-011-0672-6

    CAS  Article  Google Scholar 

  29. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    CAS  Article  PubMed  Google Scholar 

  30. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van De Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucl Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325

    CAS  Article  PubMed  Google Scholar 

  31. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. https://doi.org/10.1186/1471-2105-12-323

    CAS  Article  Google Scholar 

  32. Li YG, Song L, Liu M, Hu ZB, Wang ZT (2009) Advancement in analysis of Salviae miltiorrhizae Radix et Rhizoma (Danshen). J Chromatogr A 1216:1941–1953. https://doi.org/10.1016/j.chroma.2008.12.032

    CAS  Article  PubMed  Google Scholar 

  33. Li J, Han G, Sun C, Sui N (2019) Research advances of MYB transcription factors in plant stress resistance and breeding. Plant Signal Behav 14:1613131. https://doi.org/10.1080/15592324.2019.1613131

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Li H, Guan H, Zhuo Q, Wang Z, Li S, Si J, Zhang B, Feng B, Kong LA, Wang F, Wang Z, Zhang L (2020) Genome-wide characterization of the abscisic acid-, stress- and ripening-induced (ASR) gene family in wheat (Triticum aestivum L.). Biol Res 53:23. https://doi.org/10.1186/s40659-020-00291-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    CAS  Article  PubMed  Google Scholar 

  36. Okrent RA, Wildermuth MC (2011) Evolutionary history of the GH3 family of acyl adenylases in rosids. Plant Mol Biol 76:489–505. https://doi.org/10.1007/s11103-011-9776-y

    CAS  Article  PubMed  Google Scholar 

  37. Pauwels L, Inze D, Goossens A (2009) Jasmonate-inducible gene: what does it mean? Trends Plant Sci 14:87–91. https://doi.org/10.1016/j.tplants.2008.11.005

    CAS  Article  PubMed  Google Scholar 

  38. Pinto RT, Freitas NC, Maximo WPF, Cardoso TB, Prudente DO, Paiva LV (2019) Genome-wide analysis, transcription factor network approach and gene expression profile of GH3 genes over early somatic embryogenesis in Coffea spp. BMC Genom 20:812. https://doi.org/10.1186/s12864-019-6176-1

    CAS  Article  Google Scholar 

  39. Singh VK, Jain M, Garg R (2014) Genome-wide analysis and expression profiling suggest diverse roles of GH3 genes during development and abiotic stress responses in legumes. Front Plant Sci 5:789. https://doi.org/10.3389/fpls.2014.00789

    Article  PubMed  Google Scholar 

  40. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127. https://doi.org/10.1105/tpc.104.023549

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415. https://doi.org/10.1105/tpc.000885

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627. https://doi.org/10.1105/tpc.104.026690

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Subramanian B, Gao S, Lercher MJ, Hu S, Chen WH (2019) Evolview v3: a webserver for visualization, annotation, and management of phylogenetic trees. Nucl Acids Res 47:W270–W275. https://doi.org/10.1093/nar/gkz357

    CAS  Article  PubMed  Google Scholar 

  44. Sun R, Wang S, Ma D, Li Y, Liu C (2019) Genome-wide analysis of cotton auxin early response gene families and their roles in somatic embryogenesis. Genes (Basel). https://doi.org/10.3390/genes10100730

    Article  PubMed Central  Google Scholar 

  45. Sun M, Li H, Li Y, Xiang H, Liu Y, He Y, Qi M, Li T (2020) Tomato YABBY2b controls plant height through regulating indole-3-acetic acid-amido synthetase (GH3.8) expression. Plant Sci 297:110530. https://doi.org/10.1016/j.plantsci.2020.110530

    CAS  Article  PubMed  Google Scholar 

  46. Tang Y, Bao X, Zhi Y, Wu Q, Guo Y, Yin X, Zeng L, Li J, Zhang J, He W, Liu W, Wang Q, Jia C, Li Z, Liu K (2019) Overexpression of a MYB family gene, OsMYB6, increases drought and salinity stress tolerance in transgenic rice. Front Plant Sci 10:168. https://doi.org/10.3389/fpls.2019.00168

    Article  PubMed  PubMed Central  Google Scholar 

  47. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673

    CAS  Article  PubMed  Google Scholar 

  48. Tian F, Yang DC, Meng YQ, Jin J, Gao G (2020) PlantRegMap: charting functional regulatory maps in plants. Nucl Acids Res 48:D1104–D1113. https://doi.org/10.1093/nar/gkz1020

    CAS  Article  PubMed  Google Scholar 

  49. Vielba JM (2018) Identification and initial characterization of a new subgroup in the GH3 gene family in woody plants. J Plant Biochem Biotechnol 28:280–290. https://doi.org/10.1007/s13562-018-0477-3

    CAS  Article  Google Scholar 

  50. Wang X, Morris-Natschke SL, Lee KH (2007) New developments in the chemistry and biology of the bioactive constituents of Tanshen. Med Res Rev 27:133–148. https://doi.org/10.1002/med.20077

    CAS  Article  PubMed  Google Scholar 

  51. Wang H, Tian CE, Duan J, Wu KQ (2008) Research progresses on GH3s, one family of primary auxin-responsive genes. Plant Growth Regul 56:225–232. https://doi.org/10.1007/s10725-008-9313-4

    CAS  Article  Google Scholar 

  52. Wang R, Li M, Wu X, Wang J (2019) The gene structure and expression level changes of the GH3 gene family in Brassica napus relative to its diploid ancestors. Genes (Basel). https://doi.org/10.3390/genes10010058

    Article  PubMed  PubMed Central  Google Scholar 

  53. Wenping H, Yuan Z, Jie S, Lijun Z, Zhezhi W (2011) De novo transcriptome sequencing in Salvia miltiorrhiza to identify genes involved in the biosynthesis of active ingredients. Genomics 98:272–279. https://doi.org/10.1016/j.ygeno.2011.03.012

    CAS  Article  PubMed  Google Scholar 

  54. Westfall CS, Herrmann J, Chen Q, Wang S, Jez JM (2010) Modulating plant hormones by enzyme action: the GH3 family of acyl acid amido synthetases. Plant Signal Behav 5:1607–1612. https://doi.org/10.4161/psb.5.12.13941

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Westfall CS, Zubieta C, Herrmann J, Kapp U, Nanao MH, Jez JM (2012) Structural basis for prereceptor modulation of plant hormones by GH3 proteins. Science 336:1708–1711. https://doi.org/10.1126/science.1221863

    CAS  Article  PubMed  Google Scholar 

  56. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735. https://doi.org/10.1093/aob/mci083

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Xing B, Yang D, Yu H, Zhang B, Yan K, Zhang X, Han R, Liang Z (2018) Overexpression of SmbHLH10 enhances tanshinones biosynthesis in Salvia miltiorrhiza hairy roots. Plant Sci 276:229–238. https://doi.org/10.1016/j.plantsci.2018.07.016

    CAS  Article  PubMed  Google Scholar 

  58. Xu Z, Peters RJ, Weirather J, Luo H, Liao B, Zhang X, Zhu Y, Ji A, Zhang B, Hu S, Au KF, Song J, Chen S (2015) Full-length transcriptome sequences and splice variants obtained by a combination of sequencing platforms applied to different root tissues of Salvia miltiorrhiza and tanshinone biosynthesis. Plant J 82:951–961. https://doi.org/10.1111/tpj.12865

    CAS  Article  PubMed  Google Scholar 

  59. Xu H, Song J, Luo H, Zhang Y, Li Q, Zhu Y, Xu J, Li Y, Song C, Wang B, Sun W, Shen G, Zhang X, Qian J, Ji A, Xu Z, Luo X, He L, Li C, Sun C, Yan H, Cui G, Li X, Li X, Wei J, Liu J, Wang Y, Hayward A, Nelson D, Ning Z, Peters RJ, Qi X, Chen S (2016a) Analysis of the genome sequence of the medicinal plant Salvia miltiorrhiza. Mol Plant 9:949–952. https://doi.org/10.1016/j.molp.2016.03.010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. Xu Z, Ji A, Song J, Chen S (2016b) Genome-wide analysis of auxin response factor gene family members in medicinal model plant Salvia miltiorrhiza. Biol Open 5:848–857. https://doi.org/10.1242/bio.017178

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Yang Y, Yue R, Sun T, Zhang L, Chen W, Zeng H, Wang H, Shen C (2014) Genome-wide identification, expression analysis of GH3 family genes in Medicago truncatula under stress-related hormones and Sinorhizobium meliloti infection. Appl Microbiol Biotechnol 99:841–854. https://doi.org/10.1007/s00253-014-6311-5

    CAS  Article  PubMed  Google Scholar 

  62. Yang Y, Yue R, Sun T, Zhang L, Chen W, Zeng H, Wang H, Shen C (2015) Genome-wide identification, expression analysis of GH3 family genes in Medicago truncatula under stress-related hormones and Sinorhizobium meliloti infection. Appl Microbiol Biotechnol 99:841–854. https://doi.org/10.1007/s00253-014-6311-5

    CAS  Article  PubMed  Google Scholar 

  63. Yu D, Qanmber G, Lu L, Wang L, Li J, Yang Z, Liu Z, Li Y, Chen Q, Mendu V, Li F, Yang Z (2018) Genome-wide analysis of cotton GH3 subfamily II reveals functional divergence in fiber development, hormone response and plant architecture. BMC Plant Biol 18:350. https://doi.org/10.1186/s12870-018-1545-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Yu H, Jiang M, Xing B, Liang L, Zhang B, Liang Z (2020) Systematic analysis of Kelch Repeat F-box (KFB) protein family and identification of phenolic acid regulation members in Salvia miltiorrhiza Bunge. Genes. https://doi.org/10.3390/genes11050557

    Article  PubMed  PubMed Central  Google Scholar 

  65. Yuan H, Zhao K, Lei H, Shen X, Liu Y, Liao X, Li T (2013) Genome-wide analysis of the GH3 family in apple (Malus × domestica). BMC Genom 14:297. https://doi.org/10.1186/1471-2164-14-297

    CAS  Article  Google Scholar 

  66. Zhang RS, Wang YC, Wang C, Wei ZG, Xia D, Wang YF, Liu GF, Yang CP (2011) Time-course analysis of levels of indole-3-acetic acid and expression of auxin-responsive GH3 genes in Betula platyphylla. Plant Mol Biol Report 29:898–905. https://doi.org/10.1007/s11105-011-0306-5

    CAS  Article  Google Scholar 

  67. Zhang S, Yan Y, Wang B, Liang Z, Liu Y, Liu F, Qi Z (2014) Selective responses of enzymes in the two parallel pathways of rosmarinic acid biosynthetic pathway to elicitors in Salvia miltiorrhiza hairy root cultures. J Biosci Bioeng 117:645–651. https://doi.org/10.1016/j.jbiosc.2013.10.013

    CAS  Article  PubMed  Google Scholar 

  68. Zhang DF, Zhang N, Zhong T, Wang C, Xu ML, Ye JR (2016) Identification and characterization of the GH3 gene family in maize. J Integr Agric 15:249–261. https://doi.org/10.1016/S2095-3119(15)61076-0

    CAS  Article  Google Scholar 

  69. Zhang C, Zhang L, Wang D, Ma H, Liu B, Shi Z, Ma X, Chen Y, Chen Q (2018) Evolutionary history of the glycoside hydrolase 3 (GH3) family based on the sequenced genomes of 48 plants and identification of jasmonic acid-related GH3 proteins in Solanum tuberosum. Int J Mol Sci. https://doi.org/10.3390/ijms19071850

    Article  PubMed  PubMed Central  Google Scholar 

  70. Zhang Y, Ji A, Xu Z, Luo H, Song J (2019a) The AP2/ERF transcription factor SmERF128 positively regulates diterpenoid biosynthesis in Salvia miltiorrhiza. Plant Mol Biol 100:83–93. https://doi.org/10.1007/s11103-019-00845-7

    CAS  Article  PubMed  Google Scholar 

  71. Zhang YL, Zhang CL, Wang GL, Wang YX, Qi CH, Zhao Q, You CX, Li YY, Hao YJ (2019b) The R2R3 MYB transcription factor MdMYB30 modulates plant resistance against pathogens by regulating cuticular wax biosynthesis. BMC Plant Biol 19:362. https://doi.org/10.1186/s12870-019-1918-4

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  72. Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64. https://doi.org/10.1146/annurev-arplant-042809-112308

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333. https://doi.org/10.1016/j.biotechadv.2005.01.003

    CAS  Article  PubMed  Google Scholar 

  74. Zhou W, Huang Q, Wu X, Zhou Z, Ding M, Shi M, Huang F, Li S, Wang Y, Kai G (2017) Comprehensive transcriptome profiling of Salvia miltiorrhiza for discovery of genes associated with the biosynthesis of tanshinones and phenolic acids. Sci Rep 7:10554. https://doi.org/10.1038/s41598-017-10215-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by the Natural Science Foundation of Zhejiang Province (Grant No. LY18C150010), and the 521 Talent Foundation of Zhejiang Sci-Tech University.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Weibo Jin.

Ethics declarations

Conflict of interest

The authors declare that they have no direct or indirect conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Xu, J., Zhang, H. & Jin, W. Genome-wide identification, characterization, and expression profiles of auxin responsive GH3 gene family in Salvia miltiorrhiza involved in MeJA treatment. J. Plant Biochem. Biotechnol. (2021). https://doi.org/10.1007/s13562-021-00657-1

Download citation

Keywords

  • Salvia miltiorrhiza
  • GH3 family
  • Phylogenetic analysis
  • Promoter activity
  • Regulation