Trees are the oldest of living organisms on earth. For example, a great basin bristlecone pine nick-named Methuselah () living in North America turned 4770 in 2005 and therefore it is currently 4784 years old [ 12 13 ]. Several examples of bristlecone pines with an age over 4000 years are also described by Brutovská and coauthors [ 14 ]. Although this data may be arguable, reliable results showing an age over 1000 years for many trees are based on an accelerator mass spectrometry radiocarbon measurement. For example, for African baobab Grootboom (L.) it is estimated to be 1275 ± 50 years, making Grootboom the oldest known angiosperm tree with reliable dating results ( Figure 1 E) [ 9 15 ]. The maximum ages of old trees can be also found in an OLDLIST, a database of old trees: http://www.rmtrr.org/oldlist.htm

Many differences between animal and plant biology may explain a high degree of variation in their lifespan, including a combination of ecological, evolutionary, genetic, biochemical and physiological features. There is no universal definition that fully incorporates the different aspects of aging across all species. Aging of living organisms is due to the accumulation of damages to DNA, proteins and other macromolecules, resulting in deterioration of important biological functions. Aging may be considered as a program that is counterproductive for an individual, but beneficial for biological evolution due to increasing the pressure of natural selection [ 4 16 ]. In general, the rate of accumulation of such injuries depending on genes controlling DNA repair and telomere’s length should be relatively similar across organisms. However, certain differences in anatomy, physiology and biochemistry between plants and animals may define the distinction in their lifespan. Some of the biological characteristics that could explain extensive longevity are unique to trees, for example, the retention of stem-cell-like meristematic cells after each growth cycle, the aptitude to restore injured parts, generation of clones, etc., are all unique to trees [ 17 ]. Another characteristic of plants that diverge them from animals is the presence of an additional genome located in chloroplasts. Chloroplasts acquired its genome from endosymbiosis of a cyanobacterium around 1.5 billion years ago, after which there was a substantial relocation of genes from the chloroplast to the nucleus [ 18 ]. Additionally, there are several biological features that shortens the lifespan of animals and humans, which are discussed below in parts 2.3–2.5.

Amyloid fibrils are formed from monomeric proteins in the course of nucleated polymerization processes generating thermodynamically stable quaternary structures. The propensity of a protein to participate in self-assembly pathways leading to amyloid fibrils is determined by amyloidogenic regions of the protein, which might contain specific amino acid sequences that drive amyloidogenesis [ 22 ]. Such amyloids may be deposited as inclusion bodies in various tissues ( Figure 4 and Figure 5 ) [ 23 24 ], and their accumulation may lead to conformational diseases or proteopathies [ 25 27 ].

One of the features reducing the lifespan of animals and humans is concealed in the properties of a group of amyloidogenic proteins produced in their cells, as well as in cells of bacteria and fungi, but very seldom in plants [ 19 ]. Proteins synthesized on ribosomes should fold into defined three-dimensional structures in order to become functionally active. However, some proteins have an intrinsic propensity that convert them from their native functional states into either disordered aggregates or amyloids – a highly ordered insoluble cross-β-sheet fibrils ( Figure 2 and Figure 3 ) [ 19 21 ].

The ability to self-assemble into ordered amyloid-like β-sheet enriched structures is a common property shared by many polypeptides and proteins not necessarily associated with human diseases [ 22 32 ]. At the same time, unstructured protein aggregate formation is a ubiquitous process occurring across the different kingdoms of life. The accumulating data point is the possibility that one of the reasons of plant longevity may be related to the absence of amyloid-like fibrillar inclusions in their cells [ 33 ], although plants contain potentially amyloidogenic proteins [ 32 ]. The lack or very low level of amyloidogenic inclusions may be explained by the following reasons:) The absence in the plant genome of genes (or gene families) encoding proteins that possess high amyloidogenic propensity in animals and humans (part 2.8) and) the presence of inhibitors of amyloidosis in plant cells (part 2.9).

In spite of recent advances in the understanding of the amyloid fibrils structure and the mechanisms by which they are formed, there are no efficient approaches to prevent their formation and no effective treatment for conformational diseases.

Amyloidosis has been thoroughly investigated in humans, since it is often associated with human diseases. However, it often occurs in a wide variety of mammals and birds, both domesticated and living in wild nature. For example, amyloidosis has been identified as an important cause of squirrel morbidity and mortality (19.3% of deaths) [ 34 ]. It is also described in a brown hare () [ 34 ] and black-footed wild cat living in South Africa [ 35 ]. Amyloidosis is found in association with different chronic diseases in cheetah (), Siberian tigers () and mink () [ 36 ]. Old dogs develop neurodegenerative changes in the brain including cerebrovascular amyloidosis and senile plaques with amyloid deposition, containing Aβ type amyloid, the process similar to Alzheimer’s disease in humans [ 19 26 ]. Senile amyloid plaques looking similar to plaques in the Alzheimer’s disease brain of human patients are also common in old non-human primates, including African greenand Cynomolgus monkeys () [ 37 ]. Amyloidosis in animals is often associated with various diseases, for example, hepatic or renal failure, significantly shortening their lifespan [ 36 ].

Amyloidogenic properties and the ability to self-assemble were recently discovered in proteins for which these features had been difficult to suspect, expanding the group of functional amyloids. For example, Drosophila RNA binding protein Otu (Drosophila ovarian tumor) can form solid amyloid fibers in the presence of RNA [ 38 ]. Formation of amyloid fiber is directed by prion-like repeats in the intrinsically disordered C-terminal Otu domain. Remarkably, Otu possesses deubiquitinase activity, which dramatically increases as a result of protein polymerization and amyloid formation and is regulated by RNA binding. Furthermore, Otu controls excessive inflammation, delaying the aging process, and mutations in Otu shorten the longevity of Drosophila, indicating that Otu plays an important role in the extension of Drosophila lifespan [ 38 ]. Thus, some functional amyloids may play a beneficial role fulfilling important functions in an organism.

Aging-dependent formation of amyloids and amyloid-like protein aggregates causatively associates with several neurodegenerative diseases, including Parkinson’s disease, amyotrophic lateral sclerosis and other pathologies. On the other hand, some amyloidogenic proteins called “functional amyloids” formed from natively folded proteins under stringent control may fulfill diverse functional roles as structural modules, components of biofilms, extracellular matrix or even participate in RNA binding and possess enzymatic activity. They may accomplish a protective function against bacteria and viruses [ 29 30 ]. The structural advantages of such functional amyloids that allow them to be conserved in the evolution are their higher stability and resistance to proteolysis compared to monomeric forms. Some of functional amyloids possess unique physiochemical properties, which are used for surface coating and other areas of nanobiotechnology [ 31 ]. Functional amyloids are generated at any time of a lifespan, whereas pathological amyloids usually begin accumulating in individuals over their reproductive age and, therefore, there is low selective pressure for their elimination or modification.

2.7. Rare Amyloidosis in Plants

Raphanus sativus exhibit fungicidal activity [ Raphanus sativus . Interestingly, a fibril-forming capacity of this amyloid was easily manipulated by externally controlled conditions, for example, by freezing and thawing [ The formation of amyloid fibrils occurs not only in humans and animals, but also in fungi and bacteria, however, this process is very rare in plants. The authors of several publications assume that amyloid properties have not been shown under native conditions for any plant protein, although many potentially amyloidogenic proteins are present in plants [ 39 ]. The bioinformatic analysis performed using several algorithms, for example, prediction algorithms TANGO, Waltz and SARP (Sequence Analysis based on the Ranking of Probabilities) revealed that potentially amyloidogenic proteins were abundant in the proteomes of many land plants. However, in spite of the susceptibility of plant proteomes to protein aggregation, insoluble amyloid fibrils are very rare in plants [ 39 ]. It should be noted that some plant amyloidogenic proteins possess protective properties thus contributing to the prolongation of the lifespan. For example, defensins from the radishexhibit fungicidal activity [ 40 ]. Garvey and coauthors (2013) [ 40 ] examined an antifungal protein RsAFP-19 and highly amyloidogenic fragment of this protein from. Interestingly, a fibril-forming capacity of this amyloid was easily manipulated by externally controlled conditions, for example, by freezing and thawing [ 40 ].

Cocos nucifera [ Another example of the protective effect of plant amyloidogenic peptide possessing antimicrobial properties is Cn-AMP2. This 11-amino acid peptide is synthesized in the liquid endosperm of coconut, 41 ]. Cn-AMP2 possesses amyloidogenic propensity comparable with that of β-amyloid from Alzheimer’s disease plaques. In vitro Cn-AMP2 easily aggregates forming fibrillar structures with typical Congo red absorbance spectra, distinctive thioflavin T fluorescence and fibrillar morphology under TEM [ 41 ].

Prasiola linearis [42, Several authors describe rare cases of amyloidosis in plants, which occurs in specific, rather exotic cases and sites, when these proteins are used as functional amyloids to fulfil a specialized function. For example, proteinaceous, pleated β-sheet highly ordered complexes are present in extracellular polymeric substances of terrestrial alga 43 ]. These amyloid-like structures play the role of a glue for this multicellular green alga and participate in a generic mechanism ensuring mechanical strength in natural algal adhesives. The amyloid features of these structures were confirmed by a green-gold birefringence in cross-polarized light after Congo red staining, Raman spectroscopy, chemical staining, and atomic force microscopy. The structural properties of such amyloids explain an easy attachment of these microalgae to various surfaces in the urban environment [ 43 ].

Hevea brasiliensis. REF participates in natural rubber biosynthesis, contains β-sheet organized aggregates with amyloid properties proven by circular dichroism (CD), TEM, infra-red spectroscopy and X-ray diffraction [ Another example of a highly specialized amyloidogenic protein in plants is the elongation factor REF or Hevb1—a major component of latex in the “rubber tree”REF participates in natural rubber biosynthesis, contains β-sheet organized aggregates with amyloid properties proven by circular dichroism (CD), TEM, infra-red spectroscopy and X-ray diffraction [ 44 ]. Hevea is the genus of flowering plants in the spurge family used commercially for rubber production.