From Zinnia to Arabidopsis: approaching the involvement of peroxidases in lignification

Abstract

Zinnia elegans constitutes one of the most useful model systems for studying xylem differentiation, which simultaneously involves secondary cell wall synthesis, cell wall lignification, and programmed cell death. Likewise, the in vitro culture system of Z. elegans has been the best characterized as the differentiation of mesophyll cells into tracheary elements allows study of the biochemistry and physiology of xylogenesis free from the complexity that heterogeneous plant tissues impose. Moreover, Z. elegans has emerged as an excellent plant model to study the involvement of peroxidases in cell wall lignification. This is due to the simplicity and duality of the lignification pattern shown by the stems and hypocotyls, and to the basic nature of the peroxidase isoenzyme. This protein is expressed not only in hypocotyls and stems but also in mesophyll cells transdifferentiating into tracheary elements. Therefore, not only does this peroxidase fulfil all the catalytic requirements to be involved in lignification overcoming all restrictions imposed by the polymerization step, but also its expression is inherent in lignification. In fact, its basic nature is not exceptional since basic peroxidases are differentially expressed during lignification in other model systems, showing unusual and unique biochemical properties such as oxidation of syringyl moieties. This review focuses on the experiments which led to a better understanding of the lignification process in Zinnia, starting with the basic knowledge about the lignin pattern in this plant, how lignification takes place, and how a sole basic peroxidase with unusual catalytic properties is involved and regulated by hormones, H2O2, and nitric oxide.

Xylogenesis in zinnia (Zinnia elegans) cell cultures: unravelling the regulatory steps in a complex developmental programmed cell death event

“…In this experimental model the developmental program of xylem differentiation in planta is well preserved in vitro which allows reliable determination of the sequence of differentiation and cell death events, observations on the morphology of the cellular organelles, identification of signalling molecules, hormonal, molecular and gene regulatory components, examination of the architecture and chemical composition of SCWs, and investigations on intercellular communication (Hosokawa et al 2001; Pesquet et al 2003; Tokunaga et al 2005; Fukuda 2000; Novo-Uzal et al 2013). The culture is initiated from leaf mesophyll cells which can be easily separated from the other leaf tissues; it comprises a homogenous cell type and expresses high potential for synchronous transdifferentiation of the mesophyll cells yielding sufficient amounts of completed TEs.…”

“…When the vacuole collapses, the cell is dead but the released lytic enzymes proceed to degrade the protoplast debris. Moreover, the post - mortem stage (we suggest to be determined as stage IV) is featured by an active process of SCWs lignification which is non-autonomous and is supported by substances delivered from neighbouring living cells both in zinnia in vitro and in planta , and in other cell cultures and in planta systems such as differentiating xylem in Arabidopsis roots and hypocotyls of Phaseolus vulgaris (Smith et al 1994; Hosokawa et al 2001; Fukuda 2004; Tokunaga et al 2005; Avci et al 2008; Bollhöner et al 2012, 2013; Novo-Uzal et al 2013; Pesquet et al 2010, 2013). …”

“…In cooperation with ROS, NO and reactive nitrogen species may exert antioxidant and pro-oxidant as well as cell death-protecting or death-promoting effects (Delledonne et al 1998; Neill et al 2003; Wendehenne et al 2004; Iakimova and Woltering 2015). The contribution of NO to lignification and cell death of zinnia TEs has been documented by microscopy observations with NO-sensitive fluorescent probes and pharmacological studies with NO releasing and scavenging agents (Supplemental File S3, Supplemental File S4) (Gabaldón et al 2005; Gómez Ros et al 2006; Novo-Uzal et al 2013). Recently, in differentiating xylem of Populus roots, in planta , Bagniewska-Zadworna et al (2014) established contribution of NO signalling to the onset of cell differentiation and further at all stages of TEs maturation but not in the mature vessel elements.…”

A Key Role for Apoplastic H2O2 in Norway Spruce Phenolic Metabolism

“…Although there is some degree of variation among species in the architecture of the monolignol biosynthetic pathway, it is largely consistent across different plant groups (Mottiar et al, 2016). In Arabidopsis (Arabidopsis thaliana), both laccases and peroxidases are required for monolignol oxidation in lignin polymerization, possibly acting sequentially, and/or in different tissues (Berthet et al, 2011;Lee et al, 2013;Novo-Uzal et al, 2013;Zhao et al, 2013;Barros et al, 2015;Shigeto and Tsutsumi, 2016). In Norway spruce, numerous peroxidase and laccase isoenzymes have been reported in the cell walls of developing xylem and in the culture medium of the ligninforming cell culture utilized in this study (Kärkönen et al, 2002;Fagerstedt et al, 2010;Koutaniemi et al, 2015).…”

Catalytic Profile of Arabidopsis Peroxidases, AtPrx-2, 25 and 71, Contributing to Stem Lignification

“…From the similar point of view, AtPrx-2, 25, and 71 are classified to the all-round peroxidase. The structural motifs of S peroxidases, which are amino acid sequences conserved among S peroxidases but not in G peroxidases, were proposed by Ros Barceló et al (2007) [8] and Novo-Uzal et al (2013) [31]. AtPrx-2, 25, and 71 conserve, indeed, all or part of these motifs (Fig.…”