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

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.

Distinct redox state regulation in the seedling performance of Norway maple and sycamore

“…Hypocotyl growth is modulated via a transcription factor termed the elongator complex (Woloszynska et al 2018 ), which acts as a positive regulator of NAD + -induced defense responses (An et al 2016 ) and a negative regulator of the responses to oxidative stress (Zhou et al 2009 ). ROS are signaling molecules involved in regulation of developmental processes including formation of xylary elements in stem (Marzec-Schmidt et al 2020 ). ROS concentrations are regulated by a cascade of redox pairs GSH–GSSG, AsA–DHA, and modulated by NADH–NAD + and NADPH–NADP + (Kocsy et al 2013 ) involved in regulation of plant development at various growth stages (Ramakrishnan et al 2022 ).…”

Localization and Dynamics of the Methionine Sulfoxide Reductases MsrB1 and MsrB2 in Beech Seeds

“…The increased concentration of studied proteins was located in central vascular cylinder cells, primarily in outer-located areas related to developing conducting tissues, such as xylem cells, which may be associated with increased levels of ROS in these areas, as was described in aged beech seeds by Ratajczak et al [ 41 ]. ROSs exhibit a two-sided nature, playing an important signalling role in many developmental processes in plants and, in contrast, being responsible for oxidative damage to cells and even cell death, especially when the balance between ROS production and scavenging is disturbed [ 8 , 42 , 43 ]. It is suggested that the abundance of MsrBs in ROS-enriched areas corresponding to developing conductive tissues may be related to the formation of xylem because increased levels of hydrogen peroxide and superoxide anion radical were reported during the xylogenesis process in the stem and roots of Populus [ 43 ].…”

“…ROSs exhibit a two-sided nature, playing an important signalling role in many developmental processes in plants and, in contrast, being responsible for oxidative damage to cells and even cell death, especially when the balance between ROS production and scavenging is disturbed [ 8 , 42 , 43 ]. It is suggested that the abundance of MsrBs in ROS-enriched areas corresponding to developing conductive tissues may be related to the formation of xylem because increased levels of hydrogen peroxide and superoxide anion radical were reported during the xylogenesis process in the stem and roots of Populus [ 43 ]. Msrs in the central vascular cylinder may be associated with the protection of crucial enzymes, such as proteases, which are responsible for the degradation of cellular components and the formation of fully functional xylem vessels during programmed cell death accompanying xylogenesis.…”