Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation

Aroma is an important factor in fruit quality. <i>Passiflora edulis</i> (passion fruit) is popular among consumers because of its rich flavor and nutritional value. Esters are the main components of the volatile aroma of passion fruit. Lipoxygenase (LOX), as the first key enzyme upstream...

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Main Authors: Dongmei Huang, Funing Ma, Bin Wu, Wenhui Lv, Yi Xu, Wenting Xing, Di Chen, Bingqiang Xu, Shun Song
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/20/12496
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author Dongmei Huang
Funing Ma
Bin Wu
Wenhui Lv
Yi Xu
Wenting Xing
Di Chen
Bingqiang Xu
Shun Song
author_facet Dongmei Huang
Funing Ma
Bin Wu
Wenhui Lv
Yi Xu
Wenting Xing
Di Chen
Bingqiang Xu
Shun Song
author_sort Dongmei Huang
collection DOAJ
description Aroma is an important factor in fruit quality. <i>Passiflora edulis</i> (passion fruit) is popular among consumers because of its rich flavor and nutritional value. Esters are the main components of the volatile aroma of passion fruit. Lipoxygenase (LOX), as the first key enzyme upstream of esters, may play an important role in the formation of passion fruit aroma. In this study, a total of 12 passion fruit LOX (<i>PeLOX</i>) members were screened out based on the <i>Passiflora edulis</i> genome database, which were distributed unevenly on 6 chromosomes, all containing the highly conserved lipoxygenase domain and some containing the PLAT domain. The gene structure, evolutionary analysis and cis-acting elements of the family members were predicted in this study. Transcriptome analysis showed that 12 <i>PeLOX</i> genes had different degrees of response to different abiotic stresses (drought stress, salt stress, cold stress, and high temperature). <i>PeLOX1</i>, <i>PeLOX2</i>, <i>PeLOX7</i>, <i>PeLOX11</i>, and <i>PeLOX12</i> responded significantly to various abiotic stresses, while <i>PeLOX8</i> and <i>PeLOX9</i> had little change in expression in all stresses. Quantitative real-time PCR (qRT-PCR) in six tissues revealed that the 12 <i>PeLOX</i> genes exhibited tissue expression specificity, and the relative expression of most genes were particularly high in the roots, stems, and fruits. Focusing on passion fruit ripening and ester synthesis, the transcriptomic analysis showed that with the increase in fruit development and fruit maturity, the expression levels of <i>PeLOX1</i>, <i>PeLOX9</i>, <i>PeLOX11</i>, and <i>PeLOX12</i> showed downregulated expression, while <i>PeLOX2</i> and <i>PeLOX4</i> showed upregulated expression. In particular, the upregulation trend of <i>PeLOX4</i> was the most obvious, and the qRT-PCR results were consistent with the transcriptome result. Pearson correlation analysis showed that with the development and ripening of fruit, the expression level of <i>PeLOX4</i>, LOX enzyme activity and total ester content all showed an increasing trend, in particular during the period when the peel was red and shrank (from T2 to T3 stage), the esters’ contents increased by 37.4 times; the highest expression levels were all in the T3 period. The results indicated that <i>PeLOX4</i> may be a candidate gene involved in fruit ripeness and the formation of volatile aroma compounds, with the increase in fruit ripening, the expression level of <i>PeLOX4</i> increased and the LOX enzyme activity increased accordingly, thereby promoting the synthesis of volatile esters in fruit pulp. Our discovery lays the foundation for the functional study of LOX in passion fruit.
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spelling doaj.art-2c57efcc46134d0b9e0d5584aa6f78f22023-11-24T00:32:33ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-10-0123201249610.3390/ijms232012496Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester FormationDongmei Huang0Funing Ma1Bin Wu2Wenhui Lv3Yi Xu4Wenting Xing5Di Chen6Bingqiang Xu7Shun Song8Key Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaSchool of Tropical Crops, Yunnan Agricultural University, Puer 665000, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Genetic Improvement of Bananas, Haikou Experimental Station/Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute of Chinese Academy of Tropical Agricultural Sciences, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaAroma is an important factor in fruit quality. <i>Passiflora edulis</i> (passion fruit) is popular among consumers because of its rich flavor and nutritional value. Esters are the main components of the volatile aroma of passion fruit. Lipoxygenase (LOX), as the first key enzyme upstream of esters, may play an important role in the formation of passion fruit aroma. In this study, a total of 12 passion fruit LOX (<i>PeLOX</i>) members were screened out based on the <i>Passiflora edulis</i> genome database, which were distributed unevenly on 6 chromosomes, all containing the highly conserved lipoxygenase domain and some containing the PLAT domain. The gene structure, evolutionary analysis and cis-acting elements of the family members were predicted in this study. Transcriptome analysis showed that 12 <i>PeLOX</i> genes had different degrees of response to different abiotic stresses (drought stress, salt stress, cold stress, and high temperature). <i>PeLOX1</i>, <i>PeLOX2</i>, <i>PeLOX7</i>, <i>PeLOX11</i>, and <i>PeLOX12</i> responded significantly to various abiotic stresses, while <i>PeLOX8</i> and <i>PeLOX9</i> had little change in expression in all stresses. Quantitative real-time PCR (qRT-PCR) in six tissues revealed that the 12 <i>PeLOX</i> genes exhibited tissue expression specificity, and the relative expression of most genes were particularly high in the roots, stems, and fruits. Focusing on passion fruit ripening and ester synthesis, the transcriptomic analysis showed that with the increase in fruit development and fruit maturity, the expression levels of <i>PeLOX1</i>, <i>PeLOX9</i>, <i>PeLOX11</i>, and <i>PeLOX12</i> showed downregulated expression, while <i>PeLOX2</i> and <i>PeLOX4</i> showed upregulated expression. In particular, the upregulation trend of <i>PeLOX4</i> was the most obvious, and the qRT-PCR results were consistent with the transcriptome result. Pearson correlation analysis showed that with the development and ripening of fruit, the expression level of <i>PeLOX4</i>, LOX enzyme activity and total ester content all showed an increasing trend, in particular during the period when the peel was red and shrank (from T2 to T3 stage), the esters’ contents increased by 37.4 times; the highest expression levels were all in the T3 period. The results indicated that <i>PeLOX4</i> may be a candidate gene involved in fruit ripeness and the formation of volatile aroma compounds, with the increase in fruit ripening, the expression level of <i>PeLOX4</i> increased and the LOX enzyme activity increased accordingly, thereby promoting the synthesis of volatile esters in fruit pulp. Our discovery lays the foundation for the functional study of LOX in passion fruit.https://www.mdpi.com/1422-0067/23/20/12496lipoxygenase (LOX)gene familypassion fruitexpression analysisvolatile ester
spellingShingle Dongmei Huang
Funing Ma
Bin Wu
Wenhui Lv
Yi Xu
Wenting Xing
Di Chen
Bingqiang Xu
Shun Song
Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation
International Journal of Molecular Sciences
lipoxygenase (LOX)
gene family
passion fruit
expression analysis
volatile ester
title Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation
title_full Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation
title_fullStr Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation
title_full_unstemmed Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation
title_short Genome-Wide Association and Expression Analysis of the Lipoxygenase Gene Family in <i>Passiflora edulis</i> Revealing <i>PeLOX4</i> Might Be Involved in Fruit Ripeness and Ester Formation
title_sort genome wide association and expression analysis of the lipoxygenase gene family in i passiflora edulis i revealing i pelox4 i might be involved in fruit ripeness and ester formation
topic lipoxygenase (LOX)
gene family
passion fruit
expression analysis
volatile ester
url https://www.mdpi.com/1422-0067/23/20/12496
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