Genome-wide analysis of the passion fruit invertase gene family reveals involvement of PeCWINV5 in hexose accumulation.

beta-Fructofuranosidase / genetics Passiflora / genetics Phylogeny Multigene Family Fruit / genetics Hexoses / metabolism Plant Proteins / genetics Gene Expression Regulation, Plant Genome, Plant Genes, Plant Stress, Physiological / genetics
Abiotic stress Gene family Invertase Passion fruit Sugar metabolism

Journal

BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807

Informations de publication

Date de publication:
06 Sep 2024
Historique:
received: 08 03 2024
accepted: 05 07 2024
medline: 7 9 2024
pubmed: 7 9 2024
entrez: 6 9 2024
Statut: epublish

Résumé

Invertases (INVs) are key enzymes in sugar metabolism, cleaving sucrose into glucose and fructose and playing an important role in plant development and the stress response, however, the INV gene family in passion fruit has not been systematically reported. In this study, a total of 16 PeINV genes were identified from the passion fruit genome and named according to their subcellular location and chromosome position. These include six cell wall invertase (CWINV) genes, two vacuolar invertase (VINV) genes, and eight neutral/alkaline invertase (N/AINV) genes. The gene structures, phylogenetic tree, and cis-acting elements of PeINV gene family were predicted using bioinformatics methods. Results showed that the upstream promoter region of the PeINV genes contained various response elements; particularly, PeVINV2, PeN/AINV3, PeN/AINV5, PeN/AINV6, PeN/AINV7, and PeN/AINV8 had more response elements. Additionally, the expression profiles of PeINV genes under different abiotic stresses (drought, salt, cold temperature, and high temperature) indicated that PeCWINV5, PeCWINV6, PeVINV1, PeVINV2, PeN/AINV2, PeN/AINV3, PeN/AINV6, and PeN/AINV7 responded significantly to these abiotic stresses, which was consistent with cis-acting element prediction results. Sucrose, glucose, and fructose are main soluble components in passion fruit pulp. The contents of total soluble sugar, hexoses, and sweetness index increased significantly at early stages during fruit ripening. Transcriptome data showed that with an increase in fruit development and maturity, the expression levels of PeCWINV2, PeCWINV5, and PeN/AINV3 exhibited an up-regulated trend, especially for PeCWINV5 which showed highest abundance, this correlated with the accumulation of soluble sugar and sweetness index. Transient overexpression results demonstrated that the contents of fructose, glucose and sucrose increased in the pulp of PeCWINV5 overexpressing fruit. It is speculated that this cell wall invertase gene, PeCWINV5, may play an important role in sucrose unloading and hexose accumulation. In this study, we systematically identified INV genes in passion fruit for the first time and further investigated their physicochemical properties, evolution, and expression patterns. Furthermore, we screened out a key candidate gene involved in hexose accumulation. This study lays a foundation for further study on INV genes and will be beneficial on the genetic improvement of passion fruit breeding.

Sections du résumé

BACKGROUND BACKGROUND
Invertases (INVs) are key enzymes in sugar metabolism, cleaving sucrose into glucose and fructose and playing an important role in plant development and the stress response, however, the INV gene family in passion fruit has not been systematically reported.
RESULTS RESULTS
In this study, a total of 16 PeINV genes were identified from the passion fruit genome and named according to their subcellular location and chromosome position. These include six cell wall invertase (CWINV) genes, two vacuolar invertase (VINV) genes, and eight neutral/alkaline invertase (N/AINV) genes. The gene structures, phylogenetic tree, and cis-acting elements of PeINV gene family were predicted using bioinformatics methods. Results showed that the upstream promoter region of the PeINV genes contained various response elements; particularly, PeVINV2, PeN/AINV3, PeN/AINV5, PeN/AINV6, PeN/AINV7, and PeN/AINV8 had more response elements. Additionally, the expression profiles of PeINV genes under different abiotic stresses (drought, salt, cold temperature, and high temperature) indicated that PeCWINV5, PeCWINV6, PeVINV1, PeVINV2, PeN/AINV2, PeN/AINV3, PeN/AINV6, and PeN/AINV7 responded significantly to these abiotic stresses, which was consistent with cis-acting element prediction results. Sucrose, glucose, and fructose are main soluble components in passion fruit pulp. The contents of total soluble sugar, hexoses, and sweetness index increased significantly at early stages during fruit ripening. Transcriptome data showed that with an increase in fruit development and maturity, the expression levels of PeCWINV2, PeCWINV5, and PeN/AINV3 exhibited an up-regulated trend, especially for PeCWINV5 which showed highest abundance, this correlated with the accumulation of soluble sugar and sweetness index. Transient overexpression results demonstrated that the contents of fructose, glucose and sucrose increased in the pulp of PeCWINV5 overexpressing fruit. It is speculated that this cell wall invertase gene, PeCWINV5, may play an important role in sucrose unloading and hexose accumulation.
CONCLUSION CONCLUSIONS
In this study, we systematically identified INV genes in passion fruit for the first time and further investigated their physicochemical properties, evolution, and expression patterns. Furthermore, we screened out a key candidate gene involved in hexose accumulation. This study lays a foundation for further study on INV genes and will be beneficial on the genetic improvement of passion fruit breeding.

Identifiants

DOI: 10.1186/s12870-024-05392-y PMID: 39243043
pubmed: 39243043
doi: 10.1186/s12870-024-05392-y
pii: 10.1186/s12870-024-05392-y
doi:

Substances chimiques

beta-Fructofuranosidase EC 3.2.1.26
Hexoses 0
Plant Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

836

Subventions

Organisme : Hainan Province Science and Technology Special Fund
ID : ZDYF2024XDNY154
Organisme : Guangxi Key Research and Development Program
ID : Gui Ke AB23026070
Organisme : National Natural Science Foundation of China
ID : 32260737
Organisme : Hainan Breeding Joint Research Project
ID : Passion Fruit Breeding Joint Research

Informations de copyright

© 2024. The Author(s).

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Auteurs

Dongmei Huang (D)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.

Bin Wu (B)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.

Ge Chen (G)

Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Key Laboratory of Passion fruit Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Guangxi Academy of Agricultural Sciences, Nanning, Guangxi, 530007, P.R. China.

Wenting Xing (W)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.

Yi Xu (Y)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.
Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Hainan Seed Industry Laboratory, Sanya, Hainan, 572025, P.R. China.

Funing Ma (F)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.
Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Hainan Seed Industry Laboratory, Sanya, Hainan, 572025, P.R. China.

Hongli Li (H)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.

Wenbin Hu (W)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.

Haijie Huang (H)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China.

Liu Yang (L)

Guangxi Crop Genetic Improvement and Biotechnology Laboratory, Key Laboratory of Passion fruit Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Guangxi Academy of Agricultural Sciences, Nanning, Guangxi, 530007, P.R. China. yangliutibs@126.com.

Shun Song (S)

Tropical Crops Genetic Resources Institute, National Key Laboratory for Tropical Crop Breeding / Key Laboratory of Crop Gene Resources and Germplasm Enhancement in Southern China, Ministry of Agriculture and Rual Affairs / Key Laboratory of Tropical Crops Germplasm Resources Genetic Improvement and Innovation of Hainan Province / Germplasm Repository of Passiflora, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan, 571101, P.R. China. songs@catas.cn.
Hainan Key Laboratory for Biosafety Monitoring and Molecular Breeding in Off-Season Reproduction Regions, Sanya Research Institute, Chinese Academy of Tropical Agricultural Sciences, Hainan Seed Industry Laboratory, Sanya, Hainan, 572025, P.R. China. songs@catas.cn.

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Classifications MeSH

questionsmedicales.fr › Enzymes et coenzymes › Enzymes › Hydrolases › Glycosidases › beta-Fructofuranosidase › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Eucaryotes › Viridiplantae › Streptophyta › Embryophyta › Tracheobionta › Magnoliopsida › Passifloraceae › Passiflora › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Sciences de l'information › Phylogenèse › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Famille multigénique › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Aliments et boissons › Aliments › Fruit › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Glucides › Sucres › Oses › Hexose › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines végétales › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Régulation de l'expression des gènes végétaux › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome végétal › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome végétal › Gènes de plante › Genome-wide analysis of the passion fruit...
questionsmedicales.fr › Phénomènes physiologiques › Stress physiologique › Genome-wide analysis of the passion fruit...