Diversity, distribution, development, and evolution of medullary bundles in Nyctaginaceae

Abstract

Premise Medullary bundles, i.e., vascular units in the pith, have evolved multiple times in vascular plants. However, no study has ever explored their anatomical diversity and evolution within a phylogenetic framework. Here, we investigated the development of the primary vascular system within Nyctaginaceae showing how medullary bundles diversified within the family. Methods Development of 62 species from 25 of the 31 genera of Nyctaginaceae in stem samples was thoroughly studied with light microscopy and micro‐computed tomography. Ancestral states were reconstructed using a maximum likelihood approach. Results Two subtypes of eusteles were found, the regular eustele, lacking medullary bundles, observed exclusively in representatives of Leucastereae, and the polycyclic eustele, containing medullary bundles, found in all the remaining taxa. Medullary bundles had the same origin and development, but the organization was variable and independent of phyllotaxy. Within the polycyclic eustele, medullary bundles developed first, followed by the formation of a continuous concentric procambium, which forms a ring of vascular bundles enclosing the initially formed medullary bundles. The regular eustele emerged as a synapomorphy of Leucastereae, while the medullary bundles were shown to be a symplesiomorphy for Nyctaginaceae. Conclusions Medullary bundles in Nyctaginaceae developed by a single shared pathway, that involved the departure of vascular traces from lateral organs toward the pith. These medullary bundles were encircled by a continuous concentric procambium that also constituted the polycyclic eustele, which was likely a symplesiomorphy for Nyctaginaceae with one single reversion to the regular eustele.

Linking the evolution of development of stem vascular system in Nyctaginaceae and its correlation to habit and species diversification

“…This developmental pathway begins with a polycyclic eustele (reviewed by Cunha Neto [ 23 ])—medullary bundles + continuous cylindrical procambium (CCP) (Figs. 1 A and 2 A).…”

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Fig. 8 Maximum likelihood reconstruction of ontogenetic pathways mapped with Mesquite on a phylogenetic tree of Nyctaginaceae following the same topology used by Cunha Neto et al [ 23 ]

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“…The ontogenies appeared only once, except for ontogeny 4 that evolved twice. The evolution of ontogenies 2 and 3 in members of Leucastereae is interesting, because the tribe has other morphological (e.g., type of trichomes, pollen and fruit—[ 42 , 76 , 77 ]) and vascular characters (e.g., type of stele, [ 23 ]) that are exclusive if compared to other lineages of the family. Curiously, from all stem ontogenies of Nyctaginaceae, Reichenbachia (ontogeny 3) is the only taxon following the commonly described development for successive cambia, i.e., regular eustele + regular cylinder + successive cambia [ 29 , 71 , 72 ].…”

“…To estimate the evolutionary history of ontogenetic pathways, we applied an ancestral state reconstruction using the same phylogenetic tree applied by Cunha Neto et al [ 23 ] under Maximum Likelihood (ML) assumptions as implemented in Mesquite version 3.5 [ 43 ].…”

“…The family includes herbs, shrubs, climbing plants, trees and suffrutescent species [ 21 , 22 ]. Regardless of growth forms, the stem vascular anatomy of most Nyctaginaceae is remarkable for their polycyclic eustele [ 23 ] and cambial variants that appear in mature stems [ 24 – 26 ]. Most other plant families only have cambial variants in certain clades or their lianescent taxa (Malpighiaceae [ 27 ]; Sapindaceae [ 9 , 28 ]), although they are also found in self-supporting plants derived from lianescent ancestors (Bignoniaceae [ 8 ]; Convolvulaceae [ 29 ]).…”