Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species.


Journal

BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720

Informations de publication

Date de publication:
12 05 2023
Historique:
received: 26 10 2022
accepted: 11 04 2023
medline: 15 5 2023
pubmed: 13 5 2023
entrez: 12 5 2023
Statut: epublish

Résumé

Anthocyanins, a class of specialized metabolites that are ubiquitous among plant species, have attracted a great deal of attention from plant biologists due to their chemical diversity. They confer purple, pink, and blue colors that attract pollinators, protect plants from ultraviolet (UV) radiation, and scavenge reactive oxygen species (ROS) to facilitate plant survival during abiotic stress. In a previous study, we identified Beauty Mark (BM) in Gossypium barbadense as an activator of the anthocyanin biosynthesis pathway; this gene also directly led to the formation of a pollinator-attracting purple spot. Here, we found that a single nucleotide polymorphism (SNP) (C/T) within the BM coding sequence was responsible for variations in this trait. Transient expression assays of BM from G. barbadense and G. hirsutum in Nicotiana benthamiana using luciferase reporter gene also suggested that SNPs in the coding sequence could be responsible for the absent beauty mark phenotype observed in G. hirsutum. We next demonstrated that the beauty mark and UV floral patterns are associated phenotypes and that UV exposure resulted in increased ROS generation in floral tissues; BM thus contributed to ROS scavenging in G. barbadense and wild cotton plants with flowers containing the beauty mark. Furthermore, a nucleotide diversity analysis and Tajima's D Test suggested that there have been strong selective sweeps in the GhBM locus during G. hirsutum domestication. Taken together, these results suggest that cotton species differ in their approaches to absorbing or reflecting UV light and thus exhibit variations in floral anthocyanin biosynthesis to scavenge reactive ROS; furthermore, these traits are related to the geographic distribution of cotton species.

Sections du résumé

BACKGROUND
Anthocyanins, a class of specialized metabolites that are ubiquitous among plant species, have attracted a great deal of attention from plant biologists due to their chemical diversity. They confer purple, pink, and blue colors that attract pollinators, protect plants from ultraviolet (UV) radiation, and scavenge reactive oxygen species (ROS) to facilitate plant survival during abiotic stress. In a previous study, we identified Beauty Mark (BM) in Gossypium barbadense as an activator of the anthocyanin biosynthesis pathway; this gene also directly led to the formation of a pollinator-attracting purple spot.
RESULTS
Here, we found that a single nucleotide polymorphism (SNP) (C/T) within the BM coding sequence was responsible for variations in this trait. Transient expression assays of BM from G. barbadense and G. hirsutum in Nicotiana benthamiana using luciferase reporter gene also suggested that SNPs in the coding sequence could be responsible for the absent beauty mark phenotype observed in G. hirsutum. We next demonstrated that the beauty mark and UV floral patterns are associated phenotypes and that UV exposure resulted in increased ROS generation in floral tissues; BM thus contributed to ROS scavenging in G. barbadense and wild cotton plants with flowers containing the beauty mark. Furthermore, a nucleotide diversity analysis and Tajima's D Test suggested that there have been strong selective sweeps in the GhBM locus during G. hirsutum domestication.
CONCLUSIONS
Taken together, these results suggest that cotton species differ in their approaches to absorbing or reflecting UV light and thus exhibit variations in floral anthocyanin biosynthesis to scavenge reactive ROS; furthermore, these traits are related to the geographic distribution of cotton species.

Identifiants

pubmed: 37173786
doi: 10.1186/s12915-023-01591-5
pii: 10.1186/s12915-023-01591-5
pmc: PMC10176956
doi:

Substances chimiques

Anthocyanins 0
Reactive Oxygen Species 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

106

Subventions

Organisme : National Natural Science Foundation of China
ID : 32072115

Informations de copyright

© 2023. The Author(s).

Références

Plant Cell. 1995 Jul;7(7):1085-1097
pubmed: 12242399
Trends Ecol Evol. 2013 May;28(5):307-15
pubmed: 23480953
Plant Cell. 2014 Mar;26(3):962-80
pubmed: 24642943
Plant J. 2008 Mar;53(5):814-27
pubmed: 18036197
New Phytol. 2019 Jul;223(2):705-721
pubmed: 30891753
New Phytol. 2002 Sep;155(3):349-361
pubmed: 33873306
Bioinformatics. 2011 Aug 1;27(15):2156-8
pubmed: 21653522
Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:333-359
pubmed: 15012213
Curr Opin Biotechnol. 2013 Apr;24(2):329-35
pubmed: 22901316
Nat Genet. 2016 Feb;48(2):159-66
pubmed: 26656847
New Phytol. 2010 Jun;186(4):786-793
pubmed: 20569414
Plant J. 2001 Nov;28(3):319-32
pubmed: 11722774
Brief Bioinform. 2021 Jul 20;22(4):
pubmed: 33126247
New Phytol. 2016 Jul;211(2):708-18
pubmed: 26987355
J Genet. 2007 Apr;86(1):81-4
pubmed: 17656854
Plant Biotechnol J. 2022 Apr;20(4):691-710
pubmed: 34800075
Ann Bot. 2011 Nov;108(7):1225-33
pubmed: 21880658
Plant J. 2014 Feb;77(3):367-79
pubmed: 24274116
EMBO J. 2000 Nov 15;19(22):6150-61
pubmed: 11080161
Plant Cell. 1998 Feb;10(2):135-54
pubmed: 9490739
Evolution. 2001 Jul;55(7):1269-82
pubmed: 11525452
New Phytol. 2001 Jul;151(1):237-241
pubmed: 33873384
Plant Biotechnol J. 2022 Jul;20(7):1274-1284
pubmed: 35266277
Plant J. 2008 Sep;55(6):940-53
pubmed: 18532978
Plant Cell. 2007 Nov;19(11):3805-18
pubmed: 17993626
Plant Cell. 2003 Aug;15(8):1689-703
pubmed: 12897245
Nat Ecol Evol. 2017 Oct;1(10):1502-1510
pubmed: 29185514
Ann Bot. 2007 Dec;100(7):1483-9
pubmed: 17951585
Nat Genet. 2018 Jun;50(6):803-813
pubmed: 29736016
Funct Integr Genomics. 2014 Mar;14(1):177-89
pubmed: 24306138
New Phytol. 2018 Apr;218(1):380-392
pubmed: 29369384
Plant Cell. 1999 Aug;11(8):1433-44
pubmed: 10449578
Biochem Biophys Res Commun. 2018 Apr 15;498(4):946-953
pubmed: 29548824
Bio Protoc. 2012;2(18):
pubmed: 27390754
Plant Physiol Biochem. 2013 Nov;72:21-34
pubmed: 23473981
Plant J. 2011 Mar;65(5):771-84
pubmed: 21235651
Plant Cell Environ. 2011 Jul;34(7):1176-90
pubmed: 21410713
Plant Physiol. 2008 Aug;147(4):2041-53
pubmed: 18539781
Plant Physiol. 2001 Jun;126(2):485-93
pubmed: 11402179
Nature. 2011 Jan 20;469(7330):411-4
pubmed: 21217687
Plant Physiol. 2015 Apr;167(4):1448-70
pubmed: 25659381
Plant J. 2007 Feb;49(3):414-27
pubmed: 17181777
Physiol Plant. 2013 Jun;148(2):189-99
pubmed: 23039825
EMBO J. 1987 Dec 1;6(12):3553-8
pubmed: 3428265
Mol Ecol. 2003 May;12(5):1113-24
pubmed: 12694276
Theor Appl Genet. 2009 Sep;119(5):931-7
pubmed: 19588118

Auteurs

Muhammad Ali Abid (MA)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Qi Zhou (Q)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Mubashir Abbas (M)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Haiyan He (H)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Zhigang Meng (Z)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Yuan Wang (Y)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Yunxiao Wei (Y)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Sandui Guo (S)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

Rui Zhang (R)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China. zhangrui@caas.cn.

Chengzhen Liang (C)

Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, 100081, China. liangchengzhen@caas.cn.

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Classifications MeSH