AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies

Abstract Background Eucalyptus is one of the most important fast-growing tree species in the world, and its growth and development are significantly affected by nitrogen and phosphorus. The Amino acid/auxin permease (AAAP) gene family plays key roles in long-distance amino acid transport in plants,...

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Main Authors: Jiahui Wei, Yi Han, Huiming Xu, Lichuan Deng, Lu Li, Shasha Zhang, Ting Jiang, Yunzhuo Feng, Liuyin Ma
Format: Article
Language:English
Published: BMC 2025-07-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06907-x
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author Jiahui Wei
Yi Han
Huiming Xu
Lichuan Deng
Lu Li
Shasha Zhang
Ting Jiang
Yunzhuo Feng
Liuyin Ma
author_facet Jiahui Wei
Yi Han
Huiming Xu
Lichuan Deng
Lu Li
Shasha Zhang
Ting Jiang
Yunzhuo Feng
Liuyin Ma
author_sort Jiahui Wei
collection DOAJ
description Abstract Background Eucalyptus is one of the most important fast-growing tree species in the world, and its growth and development are significantly affected by nitrogen and phosphorus. The Amino acid/auxin permease (AAAP) gene family plays key roles in long-distance amino acid transport in plants, but their evolutionary diversity and gene expression analysis in Eucalyptus grandis under nutrient deficiency stress are largely unexplored. Results This study presents the first genome-wide identification and functional characterization of 78 AAAP family genes (EgAAAPs) in Eucalyptus grandis, classified into eight subfamilies. Phylogenetic analysis of 28 species across five evolutionary stages revealed the AAAP family’s classification into three groups: Group III originating from green algae and Groups I-II from mosses. This study underscores lineage-specific expansions (e.g., Eucalyptus AAPs) and algal ancestors as pivotal drivers of functional diversification during early land plant adaptation. Structural analysis revealed subfamily-specific features, including conserved motifs, domain variations, and exon-intron heterogeneity, underpinning functional divergence. Tandem duplication dominated EgAAAP expansion, with syntenic conservation to Populus trichocarpa offering molecular insights into Myrtaceae-Salicaceae divergence. Transcriptional regulatory networks identified 166 transcription factors (MYBs, WRKYs, NACs), with subgroup-specific cis-element enrichment: WRKY binding in Group II and RGA-LIKE1 in Groups I/III, mechanistically linking phosphate/nitrogen signaling. Cross-species interaction hubs of key EgAAAPs (e.g., EgAAAP37, EgAAAP38, EgAAAP41, EgAAAP42, EgAAAP43 and EgAAAP78) with stress-responsive proteins (ABCG40, STP1), amino acid transporters (UMAMITs, CAT5/6), and metal carriers (YSLs) revealed woody plant-specific networks absent in Arabidopsis. Spatiotemporal expression profiling delineated six tissue-specific clusters and dynamic hormonal responses: SA/JA induced temporally distinct modules (early, sustained, delayed), while boron/nitrogen/phosphorus deficiency triggered subgroup- and tissue-dependent regulation. Conclusions Collectively, this study deciphers the evolutionary innovation, regulatory complexity, and functional specialization of AAAP transporters in Eucalyptus, providing a framework for understanding nutrient signaling and stress resilience in woody plants.
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spelling doaj-art-c9e2048e002b4ae29ce0883dd36b01d12025-08-20T04:01:23ZengBMCBMC Plant Biology1471-22292025-07-0125112010.1186/s12870-025-06907-xAAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficienciesJiahui Wei0Yi Han1Huiming Xu2Lichuan Deng3Lu Li4Shasha Zhang5Ting Jiang6Yunzhuo Feng7Liuyin Ma8Center for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityCenter for Genomics, College of Forestry, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry UniversityAbstract Background Eucalyptus is one of the most important fast-growing tree species in the world, and its growth and development are significantly affected by nitrogen and phosphorus. The Amino acid/auxin permease (AAAP) gene family plays key roles in long-distance amino acid transport in plants, but their evolutionary diversity and gene expression analysis in Eucalyptus grandis under nutrient deficiency stress are largely unexplored. Results This study presents the first genome-wide identification and functional characterization of 78 AAAP family genes (EgAAAPs) in Eucalyptus grandis, classified into eight subfamilies. Phylogenetic analysis of 28 species across five evolutionary stages revealed the AAAP family’s classification into three groups: Group III originating from green algae and Groups I-II from mosses. This study underscores lineage-specific expansions (e.g., Eucalyptus AAPs) and algal ancestors as pivotal drivers of functional diversification during early land plant adaptation. Structural analysis revealed subfamily-specific features, including conserved motifs, domain variations, and exon-intron heterogeneity, underpinning functional divergence. Tandem duplication dominated EgAAAP expansion, with syntenic conservation to Populus trichocarpa offering molecular insights into Myrtaceae-Salicaceae divergence. Transcriptional regulatory networks identified 166 transcription factors (MYBs, WRKYs, NACs), with subgroup-specific cis-element enrichment: WRKY binding in Group II and RGA-LIKE1 in Groups I/III, mechanistically linking phosphate/nitrogen signaling. Cross-species interaction hubs of key EgAAAPs (e.g., EgAAAP37, EgAAAP38, EgAAAP41, EgAAAP42, EgAAAP43 and EgAAAP78) with stress-responsive proteins (ABCG40, STP1), amino acid transporters (UMAMITs, CAT5/6), and metal carriers (YSLs) revealed woody plant-specific networks absent in Arabidopsis. Spatiotemporal expression profiling delineated six tissue-specific clusters and dynamic hormonal responses: SA/JA induced temporally distinct modules (early, sustained, delayed), while boron/nitrogen/phosphorus deficiency triggered subgroup- and tissue-dependent regulation. Conclusions Collectively, this study deciphers the evolutionary innovation, regulatory complexity, and functional specialization of AAAP transporters in Eucalyptus, providing a framework for understanding nutrient signaling and stress resilience in woody plants.https://doi.org/10.1186/s12870-025-06907-xEucalyptus grandisAmino acid/Auxin permeaseGene family evolutionGene expressionNitrogen deficiencyPhosphate starvation
spellingShingle Jiahui Wei
Yi Han
Huiming Xu
Lichuan Deng
Lu Li
Shasha Zhang
Ting Jiang
Yunzhuo Feng
Liuyin Ma
AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies
BMC Plant Biology
Eucalyptus grandis
Amino acid/Auxin permease
Gene family evolution
Gene expression
Nitrogen deficiency
Phosphate starvation
title AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies
title_full AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies
title_fullStr AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies
title_full_unstemmed AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies
title_short AAAP gene family evolution and transcriptional regulation in Eucalyptus grandis under nitrogen, phosphate and boron deficiencies
title_sort aaap gene family evolution and transcriptional regulation in eucalyptus grandis under nitrogen phosphate and boron deficiencies
topic Eucalyptus grandis
Amino acid/Auxin permease
Gene family evolution
Gene expression
Nitrogen deficiency
Phosphate starvation
url https://doi.org/10.1186/s12870-025-06907-x
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