Secondary phloem diversity and evolution in Bignonieae (Bignoniaceae).

Abstract

Phloem evolution has been explored in the literature across very broad scales, either for vascular plants as a whole or for major plant groups, such as the monocotyledons or the former dicotyledons. However, it has never been examined in a way that would elucidate evolutionary shifts leading to the diversification of phloem in single lineages. Therefore, the present study explores in detail the patterns of phloem evolution in the tribe Bignonieae (Bignoniaceae). This group represents a particularly good model for phloem studies since it is known to have a very conspicuous and diverse phloem. A total of 19 phloem characters were coded in 56 species from all 21 genera currently recognized in the tribe Bignonieae, accounting for phloem wedge growth and for all the anatomical cell diversity encountered in the phloem. Phloem evolution was explored by reconstructing ancestral character states using maximum-likelihood assumptions with a time-calibrated molecular phylogeny for the group. Directionality and the effect of phylogenetic transformations in the current variation of quantitative traits and evolutionary correlations of selected discrete phloem traits were also tested under a maximum-likelihood approach. Individual phloem features are quite diverse in the tribe, but generally conserved within smaller clades. Contrasting phloem patterns were found when comparing major groups, with certain lineages having the phloem marked by a background of phloem fibres where all other cells are embedded, tangentially arranged sieve tubes and sieve-tubecentric parenchyma. In contrast, other lineages exhibited a scarcely fibrous phloem, regularly stratified phloem, sieve tube elements in radial or diffuse arrangement, and diffuse parenchyma. We found signals of directional evolution in fibre abundance and number of sieve areas, which increased in the 'Fridericia and allies extended clade' and decreased in the 'Multiples of four extended clade', resulting in no signal of directionality when the whole Bignonieae was considered. In contrast, no indication of directional evolution was found for the axial parenchyma, either in single clades within Bignonieae or in the entire tribe. Positive correlation was found between sieve element length and both sieve plate type and the presence of a storied structure. Correlated evolution was also found between fibre abundance and several traits, such as sieve tube arrangement, sieve plate type, parenchyma arrangement, ray lignification and number of companion cells. The secondary phloem of Bignonieae is extremely diverse, with sister lineages exhibiting distinct phloem anatomies derived from contrasting patterns of evolution in fibre abundance. Fibre abundance in the tribe has diversified in correlation with sieve tube arrangement, sieve tube morphology, number of companion cells and parenchyma type. The results challenge long-standing hypotheses regarding general trends in cell abundance and morphological cell evolution within the phloem, and demonstrate the need to expand studies in phloem anatomy both at a narrow taxonomic scale and at a broad one, such as to families and orders.