The molecular control of tendril development in angiosperms

Abstract

The climbing habit has evolved multiple times during the evolutionary history of angiosperms. Plants evolved various strategies for climbing, such as twining stems, tendrils and hooks. Tendrils are threadlike organs with the ability to twine around other structures through helical growth; they may be derived from a variety of structures, such as branches, leaflets and inflorescences. The genetic capacity to grow as a tendrilled climber existed in some of the earliest land plants; however, the underlying molecular basis of tendril development has been studied in only a few taxa. Here, we summarize what is known about the molecular basis of tendril development in model and candidate model species from key tendrilled families, that is, Fabaceae, Vitaceae, Cucurbitaceae, Passifloraceae and Bignoniaceae. Studies on tendril molecular genetics and development show the molecular basis of tendril formation and ontogenesis is diverse, even when tendrils have the same ontogenetic origin, for example leaflet-derived tendrils in Fabaceae and Bignoniaceae. Interestingly, all tendrils perform helical growth during contact-induced coiling, indicating that such ability is not correlated with their ontogenetic origin or phylogenetic history. Whether the same genetic networks are involved during helical growth in diverse tendrils still remains to be investigated.

LMI1 homeodomain protein regulates organ proportions by spatial modulation of endoreduplication

“…Therefore, LMI1 and RCO, which are tandemly duplicated genes, largely function divergently in the leaf, consistent with their distinct expression domains (Vlad et al 2014). Our findings also raise the possibility that evolutionary tinkering with the LMI1 endoreduplication module, as described here, may underlie stipule transformations into leaf-like organs that are typical of many taxa (Darwin 1865;Sousa-Baena et al 2018). For example, Tendrilless (Tl; pea LMI1) expression in pea leaves is absent from leafy stipules but present in bladeless tendrils, where it causes growth arrest, associated with increased endoreduplication (expression in tendrils) (Supplemental Fig.…”

Convergent Evolution and the Diverse Ontogenetic Origins of Tendrils in Angiosperms

“…Detailed developmental studies of Echinocystis lobata , suggests that Cucurbitaceae tendrils are modified axillary shoots, with tendril ramifications corresponding to second-order branches (Gerrath et al, 2008 ). For a detailed review on the development and molecular regulation of tendrils in Cucurbitaceae see Sousa-Baena et al ( 2018 ). To our knowledge, ontogenetic studies on shoot-derived tendrils have only been conducted on the Cucurbitaceae, and the exact origin and anatomical structure of such tendrils is unknown for all other plant families.…”

“…Anatomical and molecular evidence support the hypothesis that Pisum tendrils are modified leaflets (Hofer et al, 2009 ). For a detailed review on development and molecular regulation of tendrils in Pisum see Sousa-Baena et al ( 2018 ). The leaflets of the bipinnate leaves of Entada scandens , another Fabaceae, can also be modified into tendrils.…”

“…Little is known about the development, origin and molecular regulation of tendrils outside Pisum (peas, Vitaceae), Cucumis (cucumber, Cucurbitaceae), and Vitis (grapevine, Vitaceae). Studies on the underlying molecular basis of tendril development suggest their molecular regulation is complex as even tendrils with the same ontogenetic origin are controlled by diverse gene networks (Sousa-Baena et al, 2018 ). Specifically, helical growth and coiling in tendrils seems to be generated by gelatinous fibers via asymmetric contraction of the fiber ribbon owing to differential desiccation (Bowling and Vaughn, 2009 ; Gerbode et al, 2012 ).…”

“…Specifically, helical growth and coiling in tendrils seems to be generated by gelatinous fibers via asymmetric contraction of the fiber ribbon owing to differential desiccation (Bowling and Vaughn, 2009 ; Gerbode et al, 2012 ). However, a possible link between changes in cytoskeletal elements and helical growth in natural climbing plants has been recently established (Smyth, 2015 ; Sousa-Baena et al, 2018 ). The ability to perform helical growth is found in ferns, gymnosperms, basal angiosperms, magnoliids, monocots, and eudicots, indicating that helical growth might actually represent a case of deep homology.…”