Comparative morphological analysis of two parallel mycoheterotrophic transitions reveals divergent and convergent traits in the genus Pyrola (Pyroleae, Ericaceae)

Abstract

The genus Pyrola includes species with different degree of mycoheterotrophy; some species possess individuals that rely on all carbon through their associations with fungi (full mycoheterotrophy, FM), whereas some species obtain carbon through both fungi and photosynthesis by itself (partial mycoheterotrophy, PM). To investigate how plant functional traits of photosynthesis and reproduction are related to the degree of mycoheterotrophy in the initial stage of the transition from PM to FM, we determined morphological traits in FM (or nearly FM) and PM species in two independent lineages, P. picta and P. japonica complexes. We used herbarium specimens and examined leaf number, leaf area, flower number, and scape length in FM or nearly FM species (P. aphylla and P. subaphylla) and PM species (P. picta s.l. and P. japonica). We found a leaf area reduction in FM (or nearly FM) species in both lineages, suggesting that this is a convergent trait. The number of flowers was not significantly different between FM (or nearly FM) and PM species in both lineages. On the other hand, differences in the variation between FM (or nearly FM) and PM species were found in some traits between the two lineages. The FM (or nearly FM) species in one lineage only possessed rudimentary leaves, whereas that in the other linage possessed a few small, ordinary leaves in addition to those with only rudimentary leaves. The scape length of the FM (or nearly FM) species was significantly longer than that of PM species in one lineage, whereas it was shorter in the other lineage. The different and common variations are divergent and convergent traits, respectively, that could be associated with the transition to FM in Pylora. In addition, shoots of both PM species occasionally lacked ordinary leaves, possibly indicating possession of these shoots is preadaptation for the transition to FM in Pyrola.

Evidence for newly discovered albino mutants in a pyroloid: implication for the nutritional mode in the genus Pyrola

“…We identified the albino population based on its chloroplast haplotype and morphology as P. japonica , a partially mycoheterotrophic species in the wild. Qualitative morphology of flowers, leaves, and scales suggests that the population belongs, at least, to the P. japonica species complex, including P. japonica and the nearly fully mycoheterotrophic P. subaphylla , with no or relatively small leaves (taxonomically defined by Shutoh et al., ). Chloroplast haplotype C, described by Shutoh et al.…”

“…Such studies should provide valuable findings in terms of comparison with the many findings obtained from Orchidaceae (e.g., Abadie et al., ; Roy et al., ; Suetsugu et al., , ; Lallemand et al., ). Further, the albino mutants were fortunately found within the P. japonica species complex, which exhibits morphological similarities and continuous leaf size variation between partially mycoheterotrophic and nearly fully mycoheterotrophic species (Shutoh et al., , ). The mutants should also play a significant role as a standard with fully mycoheterotrophic status in further studies using the P. japonica species complex (or other Pyrola species).…”

“…3.4.4. In addition, we obtained enrichment factors for P. aphylla —a fully mycoheterotrophic Pyrola distributed in North America—and P. subaphylla —a putative nearly fully mycoheterotrophic plant with limited photosynthetic ability (having no or relatively small leaves; Shutoh et al., , )—from previous studies (Hynson et al., ; Shutoh et al., ) and compared them with those of putative albino plants. Because Shutoh et al.…”

“…All shoots were white or pale reddish and never green. The genus Pyrola , along with Orchidaceae, has attracted attention as an ideal model to examine mycoheterotrophic plants because it includes both putative fully and partially mycoheterotrophic species (Selosse and Roy, ; Shutoh et al., ). However, to date, albino mutants have never been reported in this genus (Lallemand et al., ).…”

“…Consequently, we report the albino mutants of P. japonica Klenze ex Alef. (taxonomically defined by Shutoh et al., ) for the first time as those of partially mycoheterotrophic species in Ericaceae. In addition, we discuss the nutritional mode in the plant tribe Pyroleae (Ericaceae) based on our novel discovery.…”