Abstract
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.
Highlights
Aging is a universal property of multicellular organisms
We further calculated the basal area increment (BAI) every 10 y, and found that the stem BAI still maintained a high level in old trees, even up to 510 y old (Fig. 1C)
The vascular cambium, on the other hand, can ensure both increased tree girth and annual renewal of vascular tissues over a tree’s lifespan, most mature trees are increasing in girth and production of branches, but are no longer getting taller [17]
Summary
Aging is a universal property of multicellular organisms. some tree species can live for centuries or millennia, the molecular and metabolic mechanisms underlying their longevity are unclear. Our results reveal that longlived 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. Old trees are characterized by a later onset of xylogenesis, a shorter growing season, and a lower growth rate, resulting in a smaller number of xylem cells [6], suggesting that cambial meristem activity is related to age in woody plants. How aging is manifested in cambial meristems of long-lived trees remains unknown Due to their large size, relatively slow growth rate, and long generation time, classical genetic screening of long-lived trees is difficult. The development of sequencing technologies, including RNA, sRNA, and degradome sequencing, has made it possible to test the involvement of thousands of genes in a biological
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