Xylem heterochrony: an unappreciated key to angiosperm origin and diversifications

Abstract

All angiosperms can be arranged along a spectrum from a preponderance of juvenile traits (cambial activity lost) to one of nearly all adult characters (cambium maximally active, mature patterns realized rapidly early in ontogeny). Angiosperms are unique among seed plants in the width of this spectrum. Xylem patterns are considered here to be indicative of contemporary function, not relictual. Nevertheless, most families of early-divergent angiosperms exhibit paedomorphic xylem structure, a circumstance that is most plausibly explained by the concept that early angiosperms had sympodial growth forms featuring limited accumulation of secondary xylem. Sympodial habits have been retained in various ways not only in early-divergent angiosperms, but also among eudicots in Ranunculales. The early angiosperm vessel, relatively marginal in conductive abilities, was improved in various ways, with concurrent redesign of parenchyma and fibre systems to enhance conductive, storage and mechanical capabilities. Flexibility in degree of cambial activity and kinds of juvenile/adult expressions has been basic to diversification in eudicots as a whole. Sympodial growth that lacks cambium, such as in monocots, provides advantages by various features, such as organographic compartmentalization of tracheid and vessel types. Woody monopodial eudicots were able to diversify as a result of production of new solutions to embolism prevention and conductive efficiency, particularly in vessel design, but also in parenchyma histology. Criteria for paedomorphosis in wood include slow decrease in length of fusiform cambial initials, predominance of procumbent ray cells and lesser degrees of cambial activity. Retention of ancestral features in primary xylem (the 'refugium' effect) is, in effect, a sort of inverse evidence of acceleration of adult patterns in later formed xylem. Xylem heterochrony is analysed not only for all key groups of angiosperms (including monocots), but also for different growth forms, such as lianas, annuals, various types of perennials, rosette trees and stem succulents. Xylary phenomena that potentially could be confused with heterochrony are discussed. Heterochronous xylem features seem at least as important as other often cited factors (pollination biology) because various degrees of paedomorphic xylem are found in so many growth forms that relate in xylary terms to ecological sites. Xylem heterochrony can probably be accessed during evolution by relatively simple gene changes in a wide range of angiosperms and thus represents a current as well as a past source of variation upon which diversification was based. Results discussed here are compatible with both current molecular-based phylogenetic analyses and all recent physiological work on conduction in xylem and thus represent an integration of these fields.

A review of the plants of the Princeton chert (Eocene, British Columbia, Canada)

“…One possibility is the recently described Saururus tuckerae, a plant whose modern counterpart grows today extensively along marginal aquatic zones. Stem anatomy, leaves, and wood anatomical structure of extant Saururus bear some reasonable similarities to Eorhiza Carlquist et al 1995;Carlquist 2009Carlquist , 2013Isnard et al 2012;Trueba et al 2015). A reassessment of these and some other Princeton chert plants, in light of recent knowledge about phylogenies, may help us better understand the plants that grew in this Eocene wetlands of the Okanagan Highlands and the paleoenvironment they represent.…”

Physiological and Genomic Basis of Mechanical-Functional Trade-Off in Plant Vasculature

“…There are distinct similarities between woody dicots and Arabidopsis inflorescence stems with respect to vessel length and diameter as well as presence of simple perforation plates and border Hacke et al, 2006;Schweingruber, 2006;Wheeler et al, 2007;Christman and Sperry, 2010). It has a genetic potential to develop ray cells and rayless wood is observed in juvenile trees (Carlquist, 2009;Dulin and Kirchoff, 2010). Having Arabidopsis as a full proof model for woodiness may open numerous possibilities.…”

Structural features of species of Asteraceae that arouse discussions about adaptation to seasonally dry environments of the Neotropics

“…Such patterns include variation in vessel length, diameter and frequency; type of perforation plate; and axial and radial parenchyma with storage substances, among other features, which are mainly apparent in arboreal species (Kraus et al 2007;Carlquist 2009;Yang et al 2010), However, such tissues patterns in species of the herbaceous-subshrub stratum of most biomes is poorly known. Th e main challenge faced by anatomists is determining which anatomical changes are environmentally induced and which are a result of genetic alterations, which provides crucial anatomical responses and the interpretation of the adaptations of species to their environment (Metcalfe & Chalk 1979;Kraus et al 2010;Scremin-Dias et al 2011).…”