Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants

Abstract In contrast to most land plant species, sorbitol, instead of sucrose, is the major photosynthetic product in many Rosaceae species. It has been well illustrated that three key functional genes encoding sorbitol-6-phosphate dehydrogenase (S6PDH), sorbitol dehydrogenase (SDH), and sorbitol tr...

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Main Authors: Leiting Li, Meng Li, Juyou Wu, Hao Yin, Jim M. Dunwell, Shaoling Zhang
Format: Article
Language:English
Published: BMC 2022-07-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-022-03729-z
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author Leiting Li
Meng Li
Juyou Wu
Hao Yin
Jim M. Dunwell
Shaoling Zhang
author_facet Leiting Li
Meng Li
Juyou Wu
Hao Yin
Jim M. Dunwell
Shaoling Zhang
author_sort Leiting Li
collection DOAJ
description Abstract In contrast to most land plant species, sorbitol, instead of sucrose, is the major photosynthetic product in many Rosaceae species. It has been well illustrated that three key functional genes encoding sorbitol-6-phosphate dehydrogenase (S6PDH), sorbitol dehydrogenase (SDH), and sorbitol transporter (SOT), are mainly responsible for the synthesis, degradation and transportation of sorbitol. In this study, the genome-wide identification of S6PDH, SDH and SOT genes was conducted in four Rosaceae species, peach, mei, apple and pear, and showed the sorbitol bio-pathway to be dominant (named sorbitol present group, SPG); another three related species, including tomato, poplar and Arabidopsis, showed a non-sorbitol bio-pathway (named sorbitol absent group, SAG). To understand the evolutionary differences of the three important gene families between SAG and SPG, their corresponding gene duplication, evolutionary rate, codon bias and positive selection patterns have been analyzed and compared. The sorbitol pathway genes in SPG were found to be expanded through dispersed and tandem gene duplications. Branch-specific model analyses revealed SDH and S6PDH clade A were under stronger purifying selection in SPG. A higher frequency of optimal codons was found in S6PDH and SDH than that of SOT in SPG, confirming the purifying selection effect on them. In addition, branch-site model analyses revealed SOT genes were under positive selection in SPG. Expression analyses showed diverse expression patterns of sorbitol-related genes. Overall, these findings provide new insights in the evolutionary characteristics for the three key sorbitol metabolism-related gene families in Rosaceae and other non-sorbitol dominant pathway species.
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spelling doaj.art-eb5acc393dcb49a7ab5de59507c586502022-12-22T02:12:04ZengBMCBMC Plant Biology1471-22292022-07-0122111310.1186/s12870-022-03729-zGenome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plantsLeiting Li0Meng Li1Juyou Wu2Hao Yin3Jim M. Dunwell4Shaoling Zhang5College of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversityCollege of Horticulture, Nanjing Agricultural UniversitySchool of Agriculture, Policy and Development, University of ReadingCollege of Horticulture, Nanjing Agricultural UniversityAbstract In contrast to most land plant species, sorbitol, instead of sucrose, is the major photosynthetic product in many Rosaceae species. It has been well illustrated that three key functional genes encoding sorbitol-6-phosphate dehydrogenase (S6PDH), sorbitol dehydrogenase (SDH), and sorbitol transporter (SOT), are mainly responsible for the synthesis, degradation and transportation of sorbitol. In this study, the genome-wide identification of S6PDH, SDH and SOT genes was conducted in four Rosaceae species, peach, mei, apple and pear, and showed the sorbitol bio-pathway to be dominant (named sorbitol present group, SPG); another three related species, including tomato, poplar and Arabidopsis, showed a non-sorbitol bio-pathway (named sorbitol absent group, SAG). To understand the evolutionary differences of the three important gene families between SAG and SPG, their corresponding gene duplication, evolutionary rate, codon bias and positive selection patterns have been analyzed and compared. The sorbitol pathway genes in SPG were found to be expanded through dispersed and tandem gene duplications. Branch-specific model analyses revealed SDH and S6PDH clade A were under stronger purifying selection in SPG. A higher frequency of optimal codons was found in S6PDH and SDH than that of SOT in SPG, confirming the purifying selection effect on them. In addition, branch-site model analyses revealed SOT genes were under positive selection in SPG. Expression analyses showed diverse expression patterns of sorbitol-related genes. Overall, these findings provide new insights in the evolutionary characteristics for the three key sorbitol metabolism-related gene families in Rosaceae and other non-sorbitol dominant pathway species.https://doi.org/10.1186/s12870-022-03729-zPhotosynthesis productRosaceaeSorbitol-6-phosphate dehydrogenase (S6PDH)Sorbitol dehydrogenase (SDH)Sorbitol transporter (SOT)
spellingShingle Leiting Li
Meng Li
Juyou Wu
Hao Yin
Jim M. Dunwell
Shaoling Zhang
Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants
BMC Plant Biology
Photosynthesis product
Rosaceae
Sorbitol-6-phosphate dehydrogenase (S6PDH)
Sorbitol dehydrogenase (SDH)
Sorbitol transporter (SOT)
title Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants
title_full Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants
title_fullStr Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants
title_full_unstemmed Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants
title_short Genome-wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four Rosaceae species and three model plants
title_sort genome wide identification and comparative evolutionary analysis of sorbitol metabolism pathway genes in four rosaceae species and three model plants
topic Photosynthesis product
Rosaceae
Sorbitol-6-phosphate dehydrogenase (S6PDH)
Sorbitol dehydrogenase (SDH)
Sorbitol transporter (SOT)
url https://doi.org/10.1186/s12870-022-03729-z
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