Allies or Enemies: The Role of Reactive Oxygen Species in Developmental Processes of Black Cottonwood (Populus trichocarpa).

Natalia Wojciechowska,Agnieszka Ludwików,Agnieszka Bagniewska-Zadworna,Klaudia Nemeczek,Joanna Mucha,Katarzyna Marzec-Schmidt

doi:10.3390/antiox9030199

Natalia Wojciechowska, Agnieszka Ludwików + Show 4 more

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https://doi.org/10.3390/antiox9030199

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Abstract

In contrast to aboveground organs (stems and leaves), developmental events and their regulation in underground organs, such as pioneer and fine roots, are quite poorly understood. The objective of the current study was to achieve a better understanding of the physiological and molecular role of reactive oxygen species (ROS) and ROS-related enzymes in the process of stem and pioneer root development in black cottonwood (Populus trichocarpa), as well as in the senescence of leaves and fine roots. Results of a transcriptomic analysis revealed that primary/secondary growth and senescence are accompanied by substantial changes in the expression of genes related to oxidative stress metabolism. We observed that some mechanisms common for above- and under-ground organs, e.g., the expression of superoxide dismutase (SOD) genes and SOD activity, declined during stems’ and pioneer roots’ development. Moreover, the localization of hydrogen peroxide (H2O2) and superoxide (O2•–) in the primary and secondary xylem of stems and pioneer roots confirms their involvement in xylem cell wall lignification and the induction of programmed cell death (PCD). H2O2 and O2•– in senescing fine roots were present in the same locations as demonstrated previously for ATG8 (AuTophaGy-related) proteins, implying their participation in cell degradation during senescence, while O2•– in older leaves was also localized similarly to ATG8 in chloroplasts, suggesting their role in chlorophagy. ROS and ROS-related enzymes play an integral role in the lignification of xylem cell walls in Populus trichocarpa, as well as the induction of PCD during xylogenesis and senescence.

Highlights

Reactive Oxygen Species (ROS) are highly reactive chemical compounds containing oxygen in their structure [1], which affect oxygen homeostasis when cells are exposed to environmental stress conditions and are responsible for oxidative damage to cells and even cell death [2]
Transcripts isolated from three developmental stages of poplar stems and pioneer roots were profiled to gain a comprehensive overview of gene expression during xylogenesis
Apart from the up-regulation of GST30 in leaves that may have a role in programmed cell death (PCD) signalling during leaf senescence, we identified the down-regulation of GST TAU9 which may be involved in reactive oxygen species (ROS)-scavenging in young leaves

Summary

Introduction

Reactive Oxygen Species (ROS) are highly reactive chemical compounds containing oxygen in their structure [1], which affect oxygen homeostasis when cells are exposed to environmental stress conditions and are responsible for oxidative damage to cells and even cell death [2]. ROS, play an important role in many developmental processes in plants, acting as signalling molecules [3,4]. Antioxidants function in both alleviating oxidative stress and the generation of ROS. Elevated levels of ROS play a role in plant development, in processes such as programmed cell death (PCD) [6]. ROS act as signalling molecules that trigger a cascade of events regulating developmental processes, such as the formation of xylary elements, including fibres, tracheids, and vessels [8,9]. ROS play a role in the regulation of leaf senescence, where they function as signal molecules that trigger a string of events leading to cell death [10].

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