Tandem gene duplications drive divergent evolution of caffeine and crocin biosynthetic pathways in plants.
Aldehyde dehydrogenases
Caffeine biosynthesis
Carotenoid cleavage dioxygenases
Coffea canephora
Crocin biosynthesis
Gardenia jasminoides
Genomics
N-Methyltransferases
UDP-glucosyltransferases
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
18 06 2020
18 06 2020
Historique:
received:
14
01
2020
accepted:
18
05
2020
entrez:
20
6
2020
pubmed:
20
6
2020
medline:
8
6
2021
Statut:
epublish
Résumé
Plants have evolved a panoply of specialized metabolites that increase their environmental fitness. Two examples are caffeine, a purine psychotropic alkaloid, and crocins, a group of glycosylated apocarotenoid pigments. Both classes of compounds are found in a handful of distantly related plant genera (Coffea, Camellia, Paullinia, and Ilex for caffeine; Crocus, Buddleja, and Gardenia for crocins) wherein they presumably evolved through convergent evolution. The closely related Coffea and Gardenia genera belong to the Rubiaceae family and synthesize, respectively, caffeine and crocins in their fruits. Here, we report a chromosomal-level genome assembly of Gardenia jasminoides, a crocin-producing species, obtained using Oxford Nanopore sequencing and Hi-C technology. Through genomic and functional assays, we completely deciphered for the first time in any plant the dedicated pathway of crocin biosynthesis. Through comparative analyses with Coffea canephora and other eudicot genomes, we show that Coffea caffeine synthases and the first dedicated gene in the Gardenia crocin pathway, GjCCD4a, evolved through recent tandem gene duplications in the two different genera, respectively. In contrast, genes encoding later steps of the Gardenia crocin pathway, ALDH and UGT, evolved through more ancient gene duplications and were presumably recruited into the crocin biosynthetic pathway only after the evolution of the GjCCD4a gene. This study shows duplication-based divergent evolution within the coffee family (Rubiaceae) of two characteristic secondary metabolic pathways, caffeine and crocin biosynthesis, from a common ancestor that possessed neither complete pathway. These findings provide significant insights on the role of tandem duplications in the evolution of plant specialized metabolism.
Sections du résumé
BACKGROUND
Plants have evolved a panoply of specialized metabolites that increase their environmental fitness. Two examples are caffeine, a purine psychotropic alkaloid, and crocins, a group of glycosylated apocarotenoid pigments. Both classes of compounds are found in a handful of distantly related plant genera (Coffea, Camellia, Paullinia, and Ilex for caffeine; Crocus, Buddleja, and Gardenia for crocins) wherein they presumably evolved through convergent evolution. The closely related Coffea and Gardenia genera belong to the Rubiaceae family and synthesize, respectively, caffeine and crocins in their fruits.
RESULTS
Here, we report a chromosomal-level genome assembly of Gardenia jasminoides, a crocin-producing species, obtained using Oxford Nanopore sequencing and Hi-C technology. Through genomic and functional assays, we completely deciphered for the first time in any plant the dedicated pathway of crocin biosynthesis. Through comparative analyses with Coffea canephora and other eudicot genomes, we show that Coffea caffeine synthases and the first dedicated gene in the Gardenia crocin pathway, GjCCD4a, evolved through recent tandem gene duplications in the two different genera, respectively. In contrast, genes encoding later steps of the Gardenia crocin pathway, ALDH and UGT, evolved through more ancient gene duplications and were presumably recruited into the crocin biosynthetic pathway only after the evolution of the GjCCD4a gene.
CONCLUSIONS
This study shows duplication-based divergent evolution within the coffee family (Rubiaceae) of two characteristic secondary metabolic pathways, caffeine and crocin biosynthesis, from a common ancestor that possessed neither complete pathway. These findings provide significant insights on the role of tandem duplications in the evolution of plant specialized metabolism.
Identifiants
pubmed: 32552824
doi: 10.1186/s12915-020-00795-3
pii: 10.1186/s12915-020-00795-3
pmc: PMC7302004
doi:
Substances chimiques
Carotenoids
36-88-4
Caffeine
3G6A5W338E
crocin
877GWI46C2
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
63Subventions
Organisme : National Natural Science Foundation of China
ID : 81973424
Pays : International
Organisme : CAMS Innovation Fund for Medical Sciences
ID : 2016-I2M-3-016
Pays : International
Organisme : EU grant DISCO
ID : 613513
Pays : International
Organisme : National Science Foundation
ID : 1442190
Pays : International
Références
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66
pubmed: 12136088
J Comput Biol. 2015 May;22(5):377-86
pubmed: 25549288
FEBS Lett. 2009 Oct 20;583(20):3303-9
pubmed: 19796637
Nature. 2013 Jun 6;498(7452):94-8
pubmed: 23665961
Genome Res. 2017 May;27(5):722-736
pubmed: 28298431
Nat Commun. 2018 Jan 2;9(1):13
pubmed: 29296019
Mol Plant. 2017 Jun 5;10(6):899-902
pubmed: 28315474
PLoS One. 2010 Mar 10;5(3):e9490
pubmed: 20224823
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Proc Natl Acad Sci U S A. 2019 Aug 20;116(34):17081-17089
pubmed: 31387975
Front Plant Sci. 2017 Apr 11;8:518
pubmed: 28443112
Plant Physiol. 2018 Feb;176(2):1410-1422
pubmed: 29233850
Gigascience. 2017 Nov 1;6(11):1-15
pubmed: 29048480
Bioinformatics. 2007 Nov 1;23(21):2947-8
pubmed: 17846036
New Phytol. 2016 Jan;209(2):650-63
pubmed: 26377696
Bioinformatics. 2011 Feb 15;27(4):578-9
pubmed: 21149342
Plant Physiol. 2013 Oct;163(2):682-95
pubmed: 23966550
BMC Evol Biol. 2012 May 11;12:64
pubmed: 22577841
Planta. 2013 Jan;237(1):189-210
pubmed: 23007552
Nat Biotechnol. 2011 May 15;29(7):644-52
pubmed: 21572440
Proc Natl Acad Sci U S A. 2016 Sep 20;113(38):10613-8
pubmed: 27638206
Mol Plant. 2018 Jul 2;11(7):983-994
pubmed: 29777775
Cancer Lett. 1991 May 1;57(2):109-14
pubmed: 2025883
Bioinformatics. 2014 May 1;30(9):1312-3
pubmed: 24451623
Nat Protoc. 2012 Mar 01;7(3):562-78
pubmed: 22383036
Plant Physiol. 2018 Jul;177(3):990-1006
pubmed: 29844227
BMC Plant Biol. 2011 Jan 26;11:24
pubmed: 21269483
Evid Based Complement Alternat Med. 2013;2013:686351
pubmed: 23634173
Mol Plant. 2016 Jun 6;9(6):949-52
pubmed: 27018390
Mol Plant. 2017 Jun 5;10(6):903-907
pubmed: 28315473
Science. 2018 Oct 19;362(6412):343-347
pubmed: 30166436
Nat Ecol Evol. 2017 Feb 06;1(3):59
pubmed: 28812732
Bioinformatics. 2016 Jul 15;32(14):2103-10
pubmed: 27153593
Trends Plant Sci. 2016 Sep;21(9):792-803
pubmed: 27344539
Bioinformatics. 2015 Oct 1;31(19):3210-2
pubmed: 26059717
Genome Res. 2008 Jan;18(1):188-96
pubmed: 18025269
Methods. 2012 Nov;58(3):268-76
pubmed: 22652625
Gigascience. 2017 Feb 1;6(2):1-13
pubmed: 28369459
BMC Bioinformatics. 2018 Nov 29;19(1):460
pubmed: 30497373
Science. 2014 Sep 5;345(6201):1181-4
pubmed: 25190796
Plant Physiol. 2008 Dec;148(4):1772-81
pubmed: 18952863
Genome Res. 2003 Sep;13(9):2178-89
pubmed: 12952885
Nucleic Acids Res. 2002 Apr 1;30(7):1575-84
pubmed: 11917018
PLoS One. 2014 Nov 19;9(11):e112963
pubmed: 25409509
Bioinformatics. 2006 May 15;22(10):1269-71
pubmed: 16543274
Nat Biotechnol. 2013 Dec;31(12):1119-25
pubmed: 24185095
Plant Cell. 2017 Oct;29(10):2336-2348
pubmed: 29025960
J Food Drug Anal. 2017 Jan;25(1):43-61
pubmed: 28911543
Science. 2014 May 2;344(6183):510-3
pubmed: 24786077
Proc Natl Acad Sci U S A. 2014 Aug 19;111(33):12246-51
pubmed: 25097262
New Phytol. 2015 Jun;206(4):1513-26
pubmed: 25690717
Fitoterapia. 2010 Jun;81(4):269-73
pubmed: 19815056
Plant J. 2017 Jan;89(2):181-194
pubmed: 27775193
Science. 1997 Aug 1;277(5326):696-9
pubmed: 9235894
Plant Physiol. 2006 Nov;142(3):1193-201
pubmed: 16980560
New Phytol. 2016 Aug;211(3):771-89
pubmed: 27112429
Bioinformatics. 2013 Nov 15;29(22):2933-5
pubmed: 24008419
Nat Genet. 2017 Jun;49(6):904-912
pubmed: 28481341
J Exp Bot. 2017 Jul 20;68(16):4663-4677
pubmed: 28981773
Planta. 2004 Oct;219(6):955-66
pubmed: 15605174
FEBS Lett. 2012 Apr 5;586(7):1055-61
pubmed: 22569263
Phytomedicine. 2018 Apr 1;43:21-27
pubmed: 29747750