Physiological mechanisms underlying extreme longevity in mountain pine trees

Abstract

Ancient trees are life history longevity winners that mostly persist in remote and environmentally harsh mountainous areas. Here, we performed a multifeature analysis in a protected mature mountain pine (Pinus uncinata) forest to identify the morphological and physiological traits that make these trees unique. We compared the physiology of meristematic and somatic tissues (apical buds and needles, respectively) from juvenile, mature young, mature old, and mature ancient trees under cold stress and non-stress conditions. We successfully identified key morphological features of extreme longevity at the organism level, as well as various growth, vigor, stress, and dormancy markers underlying extreme longevity in old and ancient trees. Results indicated that evolution has exerted selective pressure on specific physiological traits that make trees become longevity winners (<0.1% of the tree population were ancient trees, with an average trunk diameter >100 cm and an estimated age of 700 years). Traits entailing longevity not only included apical dominance loss, epicormic growth, and modular senescence, but also an extreme plasticity in both meristematic and somatic tissues (buds and leaves, respectively), as shown by various physiological markers. In conclusion, ancient trees are oddities that not only possess a unique ecological value, but also show divergent physiological behaviors selected during their evolution to allow them to cope with adversities and attain long life.

Growing old while staying young

“…On the one hand, assessments of physiological, transcriptomic, and metabolomic parameters in old trees revealed an upregulation of stress response markers, suggesting that aging trees do experience physiological stress (Pasques and Munne-Bosch, 2023 ; Wang et al, 2020 ). As a tree increases in size, it must pump more water and nutrients from the soil to maintain its biomass, which can be limiting under conditions where adequate resources are not available (Mencuccini et al, 2005 ).…”

“…Larger trees may also be more resilient due to their ability to store and access more resources and better withstand environmental stresses. Furthermore, old trees show no decline in meristem proliferation capacity and many other parameters of physiological performance, suggesting that wear and tear does not significantly affect their physiology (Pasques and Munne-Bosch, 2023 ; Wang et al, 2020 ). Compelling arguments for the view that trees and other perennial plants do not age come from demographic senescence studies that examine mortality and fertility patterns with age (Jones et al, 2014 ; Baudisch et al, 2013 ).…”

Ancient trees are essential elements for high-mountain forest conservation: Linking the longevity of trees to their ecological function

“…The ecological benefits of mature forests are explained by their singular physiological attributes. Mature stands display diminished branch densities, a higher diameter at breast height (DBH), and greater bark crevices, with singular age-related morphological features ( 4 , 5 ). An important fraction of extremely long-living old trees in mature forests presents several dead modules and may ultimately contribute (as decaying elements) to the carbon sequestration in subalpine poor soils ( 6 ).…”

“…An important fraction of extremely long-living old trees in mature forests presents several dead modules and may ultimately contribute (as decaying elements) to the carbon sequestration in subalpine poor soils ( 6 ). Old-growth forests, such as those of the Pyrenees, harbor trees with extreme longevities that are unique treeline past vestiges with the potential to be ecologically unique ( 5 , 7 , 8 ). Forest management results in homogeneous compositions and forest structures that negatively reduce the hosting biodiversity capacity ( 9 ).…”

“…Despite this, these plastic growth– and stress tolerance–related mechanisms are not enough to finally escape death, which still occurs ( 27 , 28 ). In this context, meristem indeterminacy, the protective mechanisms of stem cells, the absence of meristem and genetic senescence, the low occurrence of fixed somatic mutations, and the whole-plant plastic and adaptive mechanisms serve to defy aging by postponing and delimiting death to independent modules ( 5 , 27 – 32 ). Although evolution has provided several ways to almost attain immortality, anthropogenic disturbances threaten the distribution and occurrence of the oldest trees in the world ( 33 , 34 ).…”