Comprehensive Analysis of NAC Transcription Factors Reveals Their Evolution in Malvales and Functional Characterization of AsNAC019 and AsNAC098 in Aquilaria sinensis .

Publisher: MDPI Country of Publication: Switzerland NLM ID: 101092791 Publication Model: Electronic Cited Medium: Internet ISSN: 1422-0067 (Electronic) Linking ISSN: 14220067 NLM ISO Abbreviation: Int J Mol Sci Subsets: MEDLINE

Original Publication: Basel, Switzerland : MDPI, [2000-

Malvales* ; Thymelaeaceae*/genetics ; Thymelaeaceae*/chemistry; Transcription Factors/genetics ; Transcription Factors/metabolism ; Phylogeny ; Genes, Plant

NAC is a class of plant-specific transcription factors that are widely involved in the growth, development and (a)biotic stress response of plants. However, their molecular evolution has not been extensively studied in Malvales, especially in Aquilaria sinensis , a commercial and horticultural crop that produces an aromatic resin named agarwood. In this study, 1502 members of the NAC gene family were identified from the genomes of nine species from Malvales and three model plants. The macroevolutionary analysis revealed that whole genome duplication (WGD) and dispersed duplication (DSD) have shaped the current architectural structure of NAC gene families in Malvales plants. Then, 111 NAC genes were systemically characterized in A. sinensis . The phylogenetic analysis suggests that NAC genes in A. sinensis can be classified into 16 known clusters and four new subfamilies, with each subfamily presenting similar gene structures and conserved motifs. RNA-seq analysis showed that AsNACs presents a broad transcriptional response to the agarwood inducer. The expression patterns of 15 AsNACs in A. sinensis after injury treatment indicated that AsNAC019 and AsNAC098 were positively correlated with the expression patterns of four polyketide synthase (PKS) genes. Additionally, AsNAC019 and AsNAC098 were also found to bind with the AsPKS07 promoter and activate its transcription. This comprehensive analysis provides valuable insights into the molecular evolution of the NAC gene family in Malvales plants and highlights the potential mechanisms of AsNACs for regulating secondary metabolite biosynthesis in A. sinensis , especially for the biosynthesis of 2-(2-phenyl) chromones in agarwood.

BMC Bioinformatics. 2022 May 13;23(1):178. (PMID: 35562653)
Plant Cell Rep. 2023 Jun;42(6):1003-1024. (PMID: 37012438)
DNA Res. 2011 Aug;18(4):263-76. (PMID: 21685489)
PLoS One. 2020 Apr 10;15(4):e0231425. (PMID: 32275733)
DNA Res. 2003 Dec 31;10(6):239-47. (PMID: 15029955)
Hortic Res. 2018 Jun 1;5:31. (PMID: 29872536)
J Ethnobiol Ethnomed. 2019 Nov 27;15(1):57. (PMID: 31775790)
Nucleic Acids Res. 2019 Jul 2;47(W1):W5-W10. (PMID: 31062021)
BMC Plant Biol. 2014 Dec 10;14:351. (PMID: 25491370)
Int J Mol Sci. 2023 Jul 26;24(15):. (PMID: 37569353)
Proc Natl Acad Sci U S A. 2011 Jun 14;108(24):10004-9. (PMID: 21613568)
Front Plant Sci. 2023 Aug 30;14:1243323. (PMID: 37719219)
Nucleic Acids Res. 2020 Jan 8;48(D1):D265-D268. (PMID: 31777944)
Nucleic Acids Res. 2012 Apr;40(7):e49. (PMID: 22217600)
Plant Cell. 2002 Oct;14(10):2481-94. (PMID: 12368499)
Bioorg Chem. 2020 Jun;99:103789. (PMID: 32229346)
PLoS One. 2018 May 3;13(5):e0196953. (PMID: 29723301)
Mol Biol Evol. 2021 Dec 9;38(12):5825-5829. (PMID: 34597405)
Bioinformatics. 2015 Apr 15;31(8):1296-7. (PMID: 25504850)
Phytomedicine. 2022 Apr;98:153935. (PMID: 35104763)
Plant Commun. 2023 Mar 13;4(2):100471. (PMID: 36352791)
Int J Mol Sci. 2021 Mar 04;22(5):. (PMID: 33806406)
Front Plant Sci. 2023 Aug 21;14:1232804. (PMID: 37670854)
Sci Rep. 2021 Oct 6;11(1):19865. (PMID: 34615898)
Mol Ecol Resour. 2021 Jul;21(5):1416-1421. (PMID: 33629477)
Bioinformatics. 2013 Jun 1;29(11):1458-60. (PMID: 23539305)
Int J Biol Macromol. 2023 Jul 31;244:125290. (PMID: 37302633)
Nucleic Acids Res. 2015 Jul 1;43(W1):W39-49. (PMID: 25953851)
J Comput Biol. 2000;7(3-4):429-47. (PMID: 11108472)
Cell Res. 2009 Nov;19(11):1279-90. (PMID: 19752887)
J Mol Evol. 2002 Jun;54(6):746-53. (PMID: 12029356)
Fitoterapia. 2016 Oct;114:7-11. (PMID: 27502285)
Plant J. 2008 Dec;56(6):867-80. (PMID: 18694460)
PLoS One. 2018 Dec 14;13(12):e0209258. (PMID: 30550595)
Plant Cell Physiol. 2015 Feb;56(2):299-310. (PMID: 25535195)
BMC Plant Biol. 2017 Jan 6;17(1):6. (PMID: 28061815)
Trends Plant Sci. 2005 Feb;10(2):79-87. (PMID: 15708345)
Mol Plant. 2022 Dec 5;15(12):1841-1851. (PMID: 36307977)
Evol Bioinform Online. 2011;7:41-53. (PMID: 21697991)
Int J Biol Macromol. 2023 Jun 15;240:124436. (PMID: 37068542)
Gigascience. 2020 Mar 1;9(3):. (PMID: 32118265)
Plant Cell. 2022 Jul 4;34(7):2466-2474. (PMID: 35253876)
Genes (Basel). 2019 Dec 28;11(1):. (PMID: 31905649)
Nat Prod Rep. 2021 Mar 1;38(3):528-565. (PMID: 32990292)
Plant Physiol. 2023 Jul 3;192(3):1913-1927. (PMID: 36843134)
Plant Biotechnol J. 2023 Dec;21(12):2433-2457. (PMID: 37623750)
Nucleic Acids Res. 2021 Jul 2;49(W1):W293-W296. (PMID: 33885785)
Plant J. 2012 Apr;70(2):220-30. (PMID: 22098255)
Genome Res. 2009 Sep;19(9):1639-45. (PMID: 19541911)
Plant J. 2015 Apr;82(1):105-21. (PMID: 25688923)
Front Microbiol. 2013 Sep 03;4:248. (PMID: 24058359)
Plant Physiol Biochem. 2020 Dec;157:169-184. (PMID: 33120109)
Plant Sci. 2021 Jan;302:110718. (PMID: 33288024)
J Plant Res. 2020 Sep;133(5):727-737. (PMID: 32643054)
Science. 2000 Dec 15;290(5499):2114-7. (PMID: 11118139)
J Integr Plant Biol. 2022 Jul;64(7):1448-1461. (PMID: 35568969)
Plant Sci. 2022 Oct;323:111404. (PMID: 35914574)
Nucleic Acids Res. 2016 Jul 8;44(W1):W232-5. (PMID: 27084950)
Genome Biol. 2019 Nov 14;20(1):238. (PMID: 31727128)
Mol Cells. 2012 Sep;34(3):305-13. (PMID: 22965747)
Nat Commun. 2022 Jan 17;13(1):348. (PMID: 35039506)
Org Lett. 2016 Aug 5;18(15):3550-3. (PMID: 27399835)
Plant Cell Environ. 2014 Sep;37(9):2116-27. (PMID: 24548087)
New Phytol. 2015 Jun;206(4):1337-50. (PMID: 25385212)
Front Plant Sci. 2018 Dec 21;9:1900. (PMID: 30622549)
Mol Biol Evol. 2020 May 1;37(5):1530-1534. (PMID: 32011700)
Fitoterapia. 2023 Mar;165:105421. (PMID: 36587748)
Plant Physiol Biochem. 2013 Oct;71:11-21. (PMID: 23867599)
Bioinformatics. 2010 Oct 15;26(20):2631-2. (PMID: 20798169)
PLoS One. 2014 Jan 22;9(1):e86492. (PMID: 24466117)
Nucleic Acids Res. 1997 Sep 1;25(17):3389-402. (PMID: 9254694)
Front Plant Sci. 2019 Aug 16;10:1036. (PMID: 31475026)
PLoS One. 2010 Mar 10;5(3):e9490. (PMID: 20224823)
Genome Res. 2003 Feb;13(2):137-44. (PMID: 12566392)
Front Plant Sci. 2023 Feb 23;14:1095967. (PMID: 36909440)
Nucleic Acids Res. 2023 Jan 6;51(D1):D418-D427. (PMID: 36350672)
Physiol Mol Biol Plants. 2017 Apr;23(2):343-356. (PMID: 28461723)
Nucleic Acids Res. 2012 Jul;40(Web Server issue):W597-603. (PMID: 22661580)
Mol Biol Evol. 2006 May;23(5):887-92. (PMID: 16368775)
Mol Genet Genomics. 2016 Jun;291(3):1305-17. (PMID: 26942603)
Fitoterapia. 2020 Apr;142:104542. (PMID: 32147491)
Front Plant Sci. 2021 Oct 14;12:746908. (PMID: 34721474)
Int J Biol Macromol. 2023 Jul 31;244:125302. (PMID: 37315664)
Mol Biol Evol. 2016 Jul;33(7):1870-4. (PMID: 27004904)
Plant Signal Behav. 2014;9(4):e28889. (PMID: 24736489)
Plants (Basel). 2021 Feb 17;10(2):. (PMID: 33671285)
PLoS One. 2015 Aug 28;10(8):e0136993. (PMID: 26317631)
Eur J Biochem. 1999 Jun;262(2):247-57. (PMID: 10336605)
BMC Plant Biol. 2019 Apr 25;19(1):161. (PMID: 31023218)
Mol Biol Evol. 2000 Oct;17(10):1483-98. (PMID: 11018155)
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7. (PMID: 15034147)
IUBMB Life. 2014 Mar;66(3):156-166. (PMID: 24659537)
Nucleic Acids Res. 2017 Jan 4;45(D1):D1040-D1045. (PMID: 27924042)
BMC Genomics. 2019 Feb 6;20(1):113. (PMID: 30727951)
Plant J. 2012 Jun;70(5):831-44. (PMID: 22313226)
Fitoterapia. 2023 Mar;165:105422. (PMID: 36592638)
Phytochemistry. 2021 Nov;191:112932. (PMID: 34454170)

32171824 National Natural Science Foundation of China; 31870668 National Natural Science Foundation of China; 1630052020003 Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences; CARS-21 Earmarked Fund of China Agriculture Research System

Keywords: Aquilaria sinensis; Malvales; NAC; PKS; agarwood; evolution; transcriptional regulation

0 (Transcription Factors)

Date Created: 20231223 Date Completed: 20231225 Latest Revision: 20231225

20231225

PMC10744133

10.3390/ijms242417384

38139213