Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species
Abstract 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 ultrav...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-05-01
|
| Series: | BMC Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12915-023-01591-5 |
| _version_ | 1797827403277402112 |
|---|---|
| author | Muhammad Ali Abid Qi Zhou Mubashir Abbas Haiyan He Zhigang Meng Yuan Wang Yunxiao Wei Sandui Guo Rui Zhang Chengzhen Liang |
| author_facet | Muhammad Ali Abid Qi Zhou Mubashir Abbas Haiyan He Zhigang Meng Yuan Wang Yunxiao Wei Sandui Guo Rui Zhang Chengzhen Liang |
| author_sort | Muhammad Ali Abid |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-09T12:47:43Z |
| format | Article |
| id | doaj.art-d0243ae71b8648f7a06997c4ce9800ce |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-04-09T12:47:43Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-d0243ae71b8648f7a06997c4ce9800ce2023-05-14T11:27:48ZengBMCBMC Biology1741-70072023-05-0121111210.1186/s12915-023-01591-5Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium speciesMuhammad Ali Abid0Qi Zhou1Mubashir Abbas2Haiyan He3Zhigang Meng4Yuan Wang5Yunxiao Wei6Sandui Guo7Rui Zhang8Chengzhen Liang9Biotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesBiotechnology Research Institute, Chinese Academy of Agricultural SciencesAbstract 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.https://doi.org/10.1186/s12915-023-01591-5GossypiumBeauty MarkUV lightAnthocyaninGeographical adaptation |
| spellingShingle | Muhammad Ali Abid Qi Zhou Mubashir Abbas Haiyan He Zhigang Meng Yuan Wang Yunxiao Wei Sandui Guo Rui Zhang Chengzhen Liang Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species BMC Biology Gossypium Beauty Mark UV light Anthocyanin Geographical adaptation |
| title | Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species |
| title_full | Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species |
| title_fullStr | Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species |
| title_full_unstemmed | Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species |
| title_short | Natural variation in Beauty Mark is associated with UV-based geographical adaptation in Gossypium species |
| title_sort | natural variation in beauty mark is associated with uv based geographical adaptation in gossypium species |
| topic | Gossypium Beauty Mark UV light Anthocyanin Geographical adaptation |
| url | https://doi.org/10.1186/s12915-023-01591-5 |
| work_keys_str_mv | AT muhammadaliabid naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT qizhou naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT mubashirabbas naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT haiyanhe naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT zhigangmeng naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT yuanwang naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT yunxiaowei naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT sanduiguo naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT ruizhang naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies AT chengzhenliang naturalvariationinbeautymarkisassociatedwithuvbasedgeographicaladaptationingossypiumspecies |