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

Abstract

Main conclusion Physiological and molecular studies support the view that xylogenesis can largely be determined as a specific form of vacuolar programmed cell death (PCD). The studies in xylogenic zinnia cell culture have led to many breakthroughs in xylogenesis research and provided a background for investigations in other experimental models in vitro and in planta . This review discusses the most essential earlier and recent findings on the regulation of xylem elements differentiation and PCD in zinnia and other xylogenic systems. Xylogenesis (the formation of water conducting vascular tissue) is a paradigm of plant developmental PCD. The xylem vessels are composed of fused tracheary elements (TEs)—dead, hollow cells with patterned lignified secondary cell walls. They result from the differentiation of the procambium and cambium cells and undergo cell death to become functional post-mortem. The TE differentiation proceeds through a well-coordinated sequence of events in which differentiation and the programmed cellular demise are intimately connected. For years a classical experimental model for studies on xylogenesis was the xylogenic zinnia (Zinnia elegans) cell culture derived from leaf mesophyll cells that, upon induction by cytokinin and auxin, transdifferentiate into TEs. This cell system has been proven very efficient for investigations on the regulatory components of xylem differentiation which has led to many discoveries on the mechanisms of xylogenesis. The knowledge gained from this system has potentiated studies in other xylogenic cultures in vitro and in planta. The present review summarises the previous and latest findings on the hormonal and biochemical signalling, metabolic pathways and molecular and gene determinants underlying the regulation of xylem vessels differentiation in zinnia cell culture. Highlighted are breakthroughs achieved through the use of xylogenic systems from other species and newly introduced tools and analytical approaches to study the processes. The mutual dependence between PCD signalling and the differentiation cascade in the program of TE development is discussed.Electronic supplementary materialThe online version of this article (doi:10.1007/s00425-017-2656-1) contains supplementary material, which is available to authorized users.

Evaluation of Metaxylem Vessel Histogenesis and the Occurrence of Vessel Collapse during Early Development in Primary Roots of Zea mays ssp. mexicana: A Result of Premature Programmed Cell Death?

“…That it has a synchronized timing among the affected metaxylem vessels suggests that it might be a "control" gene. It is known that programmed cell death (PCD) is involved in the maturation of xylem tracheary elements in plants [7,10]. However, the PCD process in LMX, which takes a long time to complete growth to a large size and then develop thick secondary walls and autolyse [3,5], is not usually detected at such an early stage of development as that of the cells we observed collapsing.…”

The wound response in fresh-cut lettuce involves programmed cell death events

“…xylogenesis) are generally thought to conform to the vacuolar cell death type. However, in senescing leaves and petals and in differentiating xylem vessels distinct and similar molecular patterns and physiological processes reminiscent of necrotic cell death have also been documented (Quirino et al 2000; van Doorn and Woltering 2004, 2005, 2008; Lim et al 2007; Price et al 2008; Shibuya et al 2016; Iakimova and Woltering 2017). We support the concept that the entire process of senescence is a PCD event in which autophagy in the early phases and the final culmination of cellular demise are tightly integrated.…”

Vacuolar processing enzyme translocates to the vacuole through the autophagy pathway to induce programmed cell death

“…A large number of animal PCD pathways involve cysteine proteases called caspases (reviewed by Crawford and Wells, 2011; Miao et al, 2011; White et al, 2017). Although surveys of plant genomes have not revealed any ‘true’ caspases or close orthologs of animal caspases, proteases with activities similar to those of animal caspases have been reported during plant PCD, termed caspase-like proteases (CLPs; Woltering et al, 2002; Belenghi et al, 2004; Iakimova and Woltering, 2017). Caspase inhibitors inhibit PCD in plants, suggesting that the plant CLPs are distantly related to the caspases found in animals; alternatively, they may be unrelated proteins that have converged by evolutionary selection to have active sites that recognize the same substrates (Watanabe and Lam, 2004; Vacca et al, 2006; Bonneau et al, 2008).…”