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Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees

Aging is a universal property of multicellular organisms. Although some tree species can live for centuries or millennia, the molecular and metabolic mechanisms underlying their longevity are unclear. To address this, we investigated age-related changes in the vascular cambium from 15- to 667-y-old...

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Autores principales: Wang, Li, Cui, Jiawen, Jin, Biao, Zhao, Jianguo, Xu, Huimin, Lu, Zhaogeng, Li, Weixing, Li, Xiaoxia, Li, Linling, Liang, Eryuan, Rao, Xiaolan, Wang, Shufang, Fu, Chunxiang, Cao, Fuliang, Dixon, Richard A., Lin, Jinxing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6995005/
https://www.ncbi.nlm.nih.gov/pubmed/31932448
http://dx.doi.org/10.1073/pnas.1916548117
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author Wang, Li
Cui, Jiawen
Jin, Biao
Zhao, Jianguo
Xu, Huimin
Lu, Zhaogeng
Li, Weixing
Li, Xiaoxia
Li, Linling
Liang, Eryuan
Rao, Xiaolan
Wang, Shufang
Fu, Chunxiang
Cao, Fuliang
Dixon, Richard A.
Lin, Jinxing
author_facet Wang, Li
Cui, Jiawen
Jin, Biao
Zhao, Jianguo
Xu, Huimin
Lu, Zhaogeng
Li, Weixing
Li, Xiaoxia
Li, Linling
Liang, Eryuan
Rao, Xiaolan
Wang, Shufang
Fu, Chunxiang
Cao, Fuliang
Dixon, Richard A.
Lin, Jinxing
author_sort Wang, Li
collection PubMed
description Aging is a universal property of multicellular organisms. Although some tree species can live for centuries or millennia, the molecular and metabolic mechanisms underlying their longevity are unclear. To address this, we investigated age-related changes in the vascular cambium from 15- to 667-y-old Ginkgo biloba trees. The ring width decreased sharply during the first 100 to 200 y, with only a slight change after 200 y of age, accompanied by decreasing numbers of cambial cell layers. In contrast, average basal area increment (BAI) continuously increased with aging, showing that the lateral meristem can retain indeterminacy in old trees. The indole-3-acetic acid (IAA) concentration in cambial cells decreased with age, whereas the content of abscisic acid (ABA) increased significantly. In addition, cell division-, cell expansion-, and differentiation-related genes exhibited significantly lower expression in old trees, especially miR166 and HD-ZIP III interaction networks involved in cambial activity. Disease resistance-associated genes retained high expression in old trees, along with genes associated with synthesis of preformed protective secondary metabolites. Comprehensive evaluation of the expression of genes related to autophagy, senescence, and age-related miRNAs, together with analysis of leaf photosynthetic efficiencies and seed germination rates, demonstrated that the old trees are still in a healthy, mature state, and senescence is not manifested at the whole-plant level. Taken together, our results reveal that long-lived trees have evolved compensatory mechanisms to maintain a balance between growth and aging processes. This involves continued cambial divisions, high expression of resistance-associated genes, and continued synthetic capacity of preformed protective secondary metabolites.
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spelling pubmed-69950052020-02-05 Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees Wang, Li Cui, Jiawen Jin, Biao Zhao, Jianguo Xu, Huimin Lu, Zhaogeng Li, Weixing Li, Xiaoxia Li, Linling Liang, Eryuan Rao, Xiaolan Wang, Shufang Fu, Chunxiang Cao, Fuliang Dixon, Richard A. Lin, Jinxing Proc Natl Acad Sci U S A Biological Sciences Aging is a universal property of multicellular organisms. Although some tree species can live for centuries or millennia, the molecular and metabolic mechanisms underlying their longevity are unclear. To address this, we investigated age-related changes in the vascular cambium from 15- to 667-y-old Ginkgo biloba trees. The ring width decreased sharply during the first 100 to 200 y, with only a slight change after 200 y of age, accompanied by decreasing numbers of cambial cell layers. In contrast, average basal area increment (BAI) continuously increased with aging, showing that the lateral meristem can retain indeterminacy in old trees. The indole-3-acetic acid (IAA) concentration in cambial cells decreased with age, whereas the content of abscisic acid (ABA) increased significantly. In addition, cell division-, cell expansion-, and differentiation-related genes exhibited significantly lower expression in old trees, especially miR166 and HD-ZIP III interaction networks involved in cambial activity. Disease resistance-associated genes retained high expression in old trees, along with genes associated with synthesis of preformed protective secondary metabolites. Comprehensive evaluation of the expression of genes related to autophagy, senescence, and age-related miRNAs, together with analysis of leaf photosynthetic efficiencies and seed germination rates, demonstrated that the old trees are still in a healthy, mature state, and senescence is not manifested at the whole-plant level. Taken together, our results reveal that long-lived trees have evolved compensatory mechanisms to maintain a balance between growth and aging processes. This involves continued cambial divisions, high expression of resistance-associated genes, and continued synthetic capacity of preformed protective secondary metabolites. National Academy of Sciences 2020-01-28 2020-01-13 /pmc/articles/PMC6995005/ /pubmed/31932448 http://dx.doi.org/10.1073/pnas.1916548117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Wang, Li
Cui, Jiawen
Jin, Biao
Zhao, Jianguo
Xu, Huimin
Lu, Zhaogeng
Li, Weixing
Li, Xiaoxia
Li, Linling
Liang, Eryuan
Rao, Xiaolan
Wang, Shufang
Fu, Chunxiang
Cao, Fuliang
Dixon, Richard A.
Lin, Jinxing
Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees
title Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees
title_full Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees
title_fullStr Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees
title_full_unstemmed Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees
title_short Multifeature analyses of vascular cambial cells reveal longevity mechanisms in old Ginkgo biloba trees
title_sort multifeature analyses of vascular cambial cells reveal longevity mechanisms in old ginkgo biloba trees
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6995005/
https://www.ncbi.nlm.nih.gov/pubmed/31932448
http://dx.doi.org/10.1073/pnas.1916548117
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