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

First author: Li Wang; Affiliations: Yangzhou University (扬州大学): Yangzhou, China

Corresponding author: Jinxing Lin

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.

年龄增长是所有多细胞生物都具有的特征。尽管一些树木能够存活数个世纪或者千年，但这些物种长寿背后潜在的分子和代谢机制还不清楚。为了研究该问题，本文作者调查了从15年生到667年生的银杏的维管形成层在年龄上的变化。年轮宽度在前100-200年之内下降得十分迅速，但是在200年之后就呈现出了非常小的变化，伴随着形成层细胞层数目的减少。相反，平均的横断面积增加量（BAI）却随着年龄的增加而持续增，说明古树的侧生分生组织能够保持无限分化的能力。形成层细胞中吲哚-3-乙酸IAA的浓度随着年龄的增加而降低，而脱落酸ABA的浓度正好相反。另外，细胞分裂、细胞扩张以及分化相关的基因在古树中的表达量明显降低，尤其是参与了形成层活性调控的miR166和HD-ZIP III互作网络。疾病抗性相关的基因在古树中保持较高的表达水平，以及能够合成具有预保护性的次生代谢物的那些基因。通过对自噬、衰老、与年龄相关的miRNA相关的基因表达情况，以及对叶片光合作用效率和种子发芽率的统计分析，作者发现古树仍处于健康、成熟的状态，并未表现出整个植株水平上的衰老。综上，本文的研究揭示了长寿的林木通过演化出了一个补偿机制来维持生长与年龄之间的平衡。这种补偿机制包括了持续的形成层分裂、抗性相关基因的高表达以及预保护性次生代谢物的持续合成能力。

通讯：林金星（http://biology.bjfu.edu.cn/szdw/gjjcqnjjhdz/97897.html）

个人简介：1978-1982年，福建农林大学，学士；1986-1988年，澳大利亚国立大学，进修；1989-1992年，北京大学，博士；1992-1994年，中国科学院植物研究所，博士后。

研究方向：植物细胞与生殖生物学。

doi: https://doi.org/10.1073/pnas.1916548117

Journal: PNAS

Published date: January 13, 2020