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

Katarzyna Marzec-Schmidt,Natalia Wojciechowska,Agnieszka Bagniewska-Zadworna,Iga Smugarzewska,Aleksandra Zarzyńska-Nowak

doi:10.1007/s00425-019-03265-5

Katarzyna Marzec-Schmidt, Natalia Wojciechowska + Show 3 more

Open Access

https://doi.org/10.1007/s00425-019-03265-5

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Abstract

Main conclusionAutophagy is involved in developmentally programmed cell death and is identified during the early development of phloem, as well as xylem with a dual role, as both an inducer and executioner of cell death.The regulation of primary and secondary development of roots and stems is important for the establishment of root systems and for the overall survival of trees. The molecular and cellular basis of the autophagic processes, which are used at distinct moments during the growth of both organs, is crucial to understand the regulation of their development. To address this, we use Populus trichocarpa seedlings grown in a rhizotron system to examine the autophagy processes involved in root and stem development. To monitor the visual aspects of autophagy, transmission electron microscopy (TEM) and immunolocalization of AuTophaGy-related protein (ATG8) enabled observations of the phenomenon at a structural level. To gain further insight into the autophagy process at the protein and molecular level, we evaluated the expression of ATG gene transcripts and ATG protein levels. Alternations in the expression level of specific ATG genes and localization of ATG8 proteins were observed during the course of root or stem primary and secondary development. Specifically, ATG8 was present in the cells exhibiting autophagy, during the differentiation and early development of xylem and phloem tissues, including both xylary and extraxylary fibers. Ultrastructural observations revealed tonoplast invagination with the formation of autophagic-like bodies. Additionally, the accumulation of autophagosomes was identifiable during the differentiation of xylem in both organs, long before the commencement of cell death. Taken together, these results provide evidence in support of the dual role of autophagy in developmental PCD. A specific role of the controller of cell death, which is a committed step with the release of hydrolytic enzymes from the vacuole and final digestion of protoplast, from which there is no return once initiated, is only attributed to mega-autophagy.

Highlights

Autophagy, as an intracellular process responsible for the degradation of macromolecules, whole cytoplasmic compartments, and organelles, is perhaps best known for its participation in the process of eliminating dysfunctional, damaged, or toxic components from cells (Yoshimoto 2012)
The most relevant studies of autophagy during development concern xylogenesis, where structural and biochemical evidence of the role of dPCD in tracheary formation have been provided in Zinnia elegans suspension cultures that were forced to transdifferentiate into tracheary elements (Fukuda et al 1993, 1998; Fukuda 1996, 2000, 2004; Kuriyama and Fukuda 2006) and later confirmed in planta for Arabidopsis (Avci et al 2008; Kwon et al 2010) and Populus (Courtois-Moreau et al 2009; Bagniewska-Zadworna et al 2012, 2014a)
Few studies on programmed cell semi-death of phloem sieve cells were performed in developing caryopsis of Titicum aestivum, indicating that selective autophagy can be involved in that developmental process which does not end with cell death (Wang et al 2008; Yang et al 2015)

Summary

Introduction

As an intracellular process responsible for the degradation of macromolecules, whole cytoplasmic compartments, and organelles, is perhaps best known for its participation in the process of eliminating dysfunctional, damaged, or toxic components from cells (Yoshimoto 2012). 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. Determining exactly when and how various components of autophagy may affect tissue development resulting from dPCD has not been documented

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