Autophagy counteracts instantaneous cell death during seasonal senescence of the fine roots and leaves in Populus trichocarpa

Abstract

BackgroundSenescence, despite its destructive character, is a process that is precisely-regulated. The control of senescence is required to achieve remobilization of resources, a principle aspect of senescence. Remobilization allows plants to recapture valuable resources that would otherwise be lost to the environment with the senescing organ. Autophagy is one of the critical processes that is switched on during senescence. This evolutionarily conserved process plays dual, antagonistic roles. On the one hand, it counteracts instantaneous cell death and allows the process of remobilization to be set in motion, while on the other hand, it participates in the degradation of cellular components. Autophagy has been demonstrated to occur in many plant species during the senescence of leaves and flower petals. Little is known, however, about the senescence process in other ephemeral organs, such as fine roots, whose lifespan is also relatively short. We hypothesized that, like the case of seasonal leaf senescence, autophagy also plays a role in the senescence of fine roots, and that both processes are synchronized in their timing.ResultsWe evaluated which morphological and cytological symptoms are universal or unique in the senescence of fine roots and leaves. The results of our study confirmed that autophagy plays a key role in the senescence of fine roots, and is associated also with the process of cellular components degradation. In both organs, structures related to autophagy were observed, such as autophagic bodies and autophagosomes. The role of autophagy in the senescence of these plant organs was further confirmed by an analysis of ATG gene expression and protein detection.ConclusionsThe present study is the first one to examine molecular mechanisms associated with the senescence of fine roots, and provide evidence that can be used to determine whether senescence of fine roots can be treated as another example of developmentally programmed cell death (dPCD). Our results indicate that there is a strong similarity between the senescence of fine roots and other ephemeral organs, suggesting that this process occurs by the same autophagy-related mechanisms in all plant ephemeral organs.Electronic supplementary materialThe online version of this article (10.1186/s12870-018-1439-6) contains supplementary material, which is available to authorized users.

Reshaping of the Arabidopsis thaliana proteome landscape and co-regulation of proteins in development and immunity

“…All of these TCP-1/cpn60 proteins are homologs of the yeast and human cytosolic chaperonin CCT proteins suggesting they constitute the hardly described CCT complex in Arabidopsis and that it's abundance is tissue and developmentally specific ( growing cells which are well studied in root hairs (Rounds and Bezanilla, 2013), but are also prevalent in fast growing tissues such as the emerging inflorescence stem and flowers (Chen et al, 2009). On the other hand, autophagy, a process which also involves the formation of lytic compartments and vesicle trafficking for the degradation of cytoplasmic material is known to play an important role in senescence in leaves and other tissues (Wojciechowska et al, 2018). The proteins in cluster 11 primarily function in chloroplast biogenesis and the establishment of the functional photosynthetic machinery.…”

Occurrence of autophagy during pioneer root and stem development in Populus trichocarpa

“…A phenol-based method was used for the extraction of total protein as described by Wojciechowska et al (2018). Protein concentration was measured with a 2-D Quant Kit (GE Healthcare, Piscataway, NJ, USA) and proteins were separated by SDS-PAGE on 4-20% Mini-PROTEAN TGX precast gels (Bio-Rad), with an equal amount of protein (20 µg) in each lane.…”

“…Programmed cell death occurs during the course of developmental processes (dPCD) and also in response to exogenous factors (Kacprzyk et al 2011). Autophagy is a part of a highly regulated response to adapt to and survive adverse abiotic stress conditions (Han et al 2011;Luo et al 2017;Shangguan et al 2018;Pillajo et al 2018), biotic stresses (Liu et al 2005;Hayward et al 2009;Lenz et al 2011a;Zhou et al 2014), and senescence (Avila-Ospina et al 2014;Sobieszczuk-Nowicka et al 2018;Wojciechowska et al 2018). It can occur in the whole organism, a specific tissue, or in single cells.…”

“…As a result, macroautophagy is the most frequently studied, especially in the context of selective autophagy of particular components and the maintenance of homeostasis in plant cells (Li and Vierstra 2012;Masclaux-Daubresse 2016;Masclaux-Daubresse et al 2017;Yoshimoto and Ohsumi 2018). In plants, a principal characteristic of autophagy in PCD processes is its dual role as an initiator and executioner in PCD (Minina et al 2014;Wojciechowska et al 2018). Thus, its pro-survival and pro-death functions are recognized (Avila-Ospina et al 2014;van Doorn and Woltering 2010).…”

Genome-Wide Characterization of AspATs in Populus: Gene Expression Variation and Enzyme Activities in Response to Nitrogen Perturbations

“…Seasonal senescence leaves were harvested from plants grown in a green house. Mature leaves were sampled from three time points based on senescent phenotypes observed according to a previous study [33] and frozen samples were ground in liquid nitrogen and subjected to RNA and protein extraction, followed by qRT-PCR analyses and determination of enzyme activity.…”