Differential bud activation by a net positive root signal explains branching phenotype in prostrate clonal herbs: a model

Abstract

Regulation of branching within perennial prostrate clonal herbs differs from the annual orthotropic species, Arabidopsis and pea, as the dominant signal transported from roots is a branching promoter, not an inhibitor. Trifolium repens, an exemplar of such prostrate species, was used to investigate the interaction between roots and branch development. This study tests whether or not current knowledge when synthesized into a predictive model is sufficient to simulate the branching pattern developing on the shoot distal to a basal root. The major concepts underpinning the model are: (i) bud outgrowth (activation) is stimulated in a dose-dependent manner by branching promoter signals from roots, (ii) the distribution of this net root stimulus (NRS) is uniform throughout the shoot system distal to the basal root but declines geometrically in intensity upon continued enlargement of this shoot system, and (iii) each bud has an outgrowth potential, equal to the activation level of the apical bud in which it forms, that moderates its response to NRS. The validity of these concepts was further tested by running simulations of the branching of a phylogenetically-distanced prostrate perennial monocotyledonous species, Tradescantia fluminensis. For both species the model reasonably accounted for the observed pattern of branching. The outgrowth potential of buds plays an important role in limiting the number of hierarchies of branching that can develop on a plant. In conclusion, for both species, the model accounted for the major factors involved in the correlative regulation of branching and is possibly also pertinent for all prostrate clonal species.

A Conserved Potential Development Framework Applies to Shoots of Legume Species with Contrasting Morphogenetic Strategies

“…However, in prostrate species such as white clover, or in those with a terminal flowering (Thomas, 2003), interactions with the reproductive cycle will occur at some point, and integrating a reproductive dimension in the framework would most likely improve its robustness (e.g., Moreau et al, 2007). Similarly, the development of nodal roots has been shown to interact with shoot organogenesis in aging clover plants (Thomas et al, 2014), and a whole plant appraisal of morphogenesis, considering both shoot and root morphogenetic traits (Pagès, 2014) would deserve exploration. In any case, the set of deterministic rules identified in this study could serve as an initial benchmark for the future development of a more comprehensive framework.…”

“…Shoot morphogenesis thus arises from the initiation of new phytomers by shoot meristems, from the expansive growth of the individual organs produced and from the differentiation of support tissues. Like many other dicotyledonous plants (Seleznyova et al, 2002; Lebon et al, 2006), forage legumes are characterized by shoots with complex and highly branched structures (e.g., white clover: Thomas, 1987; Gautier et al, 2000; Thomas et al, 2014; red clover: Taylor and Quesenberry, 1996). Considerable variability of shoot development is usually observed in dense stands (Gosse et al, 1988; Van Minnebruggen et al, 2015).…”