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Review
. 2018 Apr 3:9:403.
doi: 10.3389/fpls.2018.00403. eCollection 2018.

Convergent Evolution and the Diverse Ontogenetic Origins of Tendrils in Angiosperms

Affiliations
Review

Convergent Evolution and the Diverse Ontogenetic Origins of Tendrils in Angiosperms

Mariane S Sousa-Baena et al. Front Plant Sci. .

Abstract

Climbers are abundant in tropical forests, where they constitute a major functional plant type. The acquisition of the climbing habit in angiosperms constitutes a key innovation. Successful speciation in climbers is correlated with the development of specialized climbing strategies such as tendrils, i.e., filiform organs with the ability to twine around other structures through helical growth. Tendrils are derived from a variety of morphological structures, e.g., stems, leaves, and inflorescences, and are found in various plant families. In fact, tendrils are distributed throughout the angiosperm phylogeny, from magnoliids to asterids II, making these structures a great model to study convergent evolution. In this study, we performed a thorough survey of tendrils within angiosperms, focusing on their origin and development. We identified 17 tendril types and analyzed their distribution through the angiosperm phylogeny. Some interesting patterns emerged. For instance, tendrils derived from reproductive structures are exclusively found in the Core Eudicots, except from one monocot species. Fabales and Asterales are the orders with the highest numbers of tendrilling strategies. Tendrils derived from modified leaflets are particularly common among asterids, occurring in Polemoniaceae, Bignoniaceae, and Asteraceae. Although angiosperms have a large number of tendrilled representatives, little is known about their origin and development. This work points out research gaps that should help guide future research on the biology of tendrilled species. Additional research on climbers is particularly important given their increasing abundance resulting from environmental disturbance in the tropics.

Keywords: climbing habit; helical growth; lianas; ontogenetic origin; primary homology; recurrent evolution; tendrils; vines.

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Figures

Figure 1
Figure 1
Schematic drawings illustrating the 17 tendril types classified in this work, and tendrils terminating in apical adhesive pads. (A–J) Tendrils derived from vegetative organs. (A) Tendrils derived from modified terminal leaflets. (B) Tendril derived from prolonged midrib. (C) Tendrils derived from prolonged bifurcated tips of the leaf midribs. (D) Tendrils derived from the modified petioles, representing a transitory structure that acquires functions other than climbing in later stages of leaf development. (E) Tendrils derived from a modified leaf tip. (F) Whole leaf modified into a simple tendril. (G) Tendrils derived from petiole duplication. (H) Tendrils derived from petioles that acquire the capacity for helical growth. (I) Tendrils derived from modified compound leaf rachis that acquires the capacity for helical growth, becoming voluble. (J) Tendril derived from a modified shoot. (K–Q) Tendrils derived from reproductive organs. (K) Tendrils derived from the tip of the reduced inflorescence apex. (L) Tendril derived from modified inflorescences. (M) Tendrils derived from modified inflorescence apices. (N) Tendrils derived from modified inflorescence rachis that acquires the capacity for helical growth, becoming voluble. (O) Tendrils derived from inflorescence lateral branches. (P) Tendrils derived from inflorescence peduncles. (Q) Tendril derived from flower pedicels that acquire the capacity for helical growth. (R) Tendrils terminating in apical adhesive pads.
Figure 2
Figure 2
Angiosperm phylogeny modified from Stevens (2001 onwards) to include Icacinales (following the APG IV; The Angiosperm Phylogeny Group, 2016), illustrating the distribution of tendrils with different ontogenetic origins, as well as the presence of adhesive pads, across angiosperm orders.
Figure 3
Figure 3
Tendrils derived from vegetative structures. (A–C) Tendrils derived from shoots. (A) Cucurbita pepo (Cucurbitaceae). (B) Bauhinia semibifida (Fabaceae). Image source: www.NatureLoveYou.sg. (C) Landolphia dulcis (Apocynaceae). (D–I) Tendrils derived from leaves or leaf parts. (D) Smilax sp. (Smilacaceae). Tendrils derived from the petiole. (E) Nepenthes sp. (Nepenthaceae). Detail of tendril and developing pitcher on the left. Arrowhead indicates the leaf blade from which a tendril is emerging. (F) Tendrils derived from petioles in Tropaeolum repandum (Tropaeolaceae). This image was reproduced with permission from [Wilhelm Barthlott]. (G) Whole leaf blade transformed into a tendril in Lathyrus aphaca (Fabaceae). Image source: www.flora-on.pt. (H) Triphyophyllum peltatum (Dioncophyllaceae). On the left side a detail illustrating the tendril grasping a branch. Images were reproduced with permission from [Wilhelm Barthlott]. (I) Tendrils originated from the leaf tip in Gloriosa superba (Colchicaceae). Arrows indicate tendrils. Image source of pictures in (F,H) (https://www.flickr.com/photos/lotus-salvinia).
Figure 4
Figure 4
Tendrils derived from leaf parts. (A) Tendrils derived from the leaf tip in Mutisia subulata (Asteraceae). (B) Tendril derived from a prolonged leaf midrib in Mutisia brachyanta. Images in (A,B) were reproduced with permission from [Michail Belov] (Image source: http://www.chileflora.com). (C-F) Tendrils derived from modified terminal leaflets. (C) Mutisia acuminata. (D) Pisum sativum (Fabaceae). Image source: www.flora-on.pt. (E) Dolichandra unguis-cati (Bignoniaceae). (F) Cobaea scandens (Polemoniaceae). Arrows indicate tendrils.
Figure 5
Figure 5
Tendrils derived from reproductive structures. (A,B) Petermannia cirrosa (Petermanniaceae), tendrils are modified inflorescences, note the similarity of the tendril in (B) with the inflorescence (arrowhead) in (A). Image in panel (A) was reproduced with permission from [David Tng]. Image source: https://www.flickr.com/photos/davidtng. Image in panel (B) was reproduced with permission from [Dennis Stevenson]. Image source: http://www.plantsystematics.org/imgs/dws/r/Petermanniaceae_Petermannia_cirrosa_43766.html. (C) Pacouria boliviensis, tendril is a modified inflorescence rachis (Apocynaceae). This image was reproduced with permission from [André Simões]. Image source: http://floradobrasil.jbrj.gov.br. (D–F) Tendrils are modified inflorescence branches. (D) Gouania lupuloides (Rhamnaceae). (E) Cardiospermum halicacabum (Sapindaceae). (F) Tendril is originated from the tip of the reduced inflorescence apex in Passiflora capsularis (Passifloraceae). (G–I) Whole inflorescence modified into tendrils. (G) Young tendrils of Parthenocissus tricuspidata (Vitaceae), seen in their adult form, with terminal adhesive pads, in (H). (I) Vitis vinifera (Vitaceae). This image was reproduced with permission from [Wilhelm Barthlott]. Image source: https://www.flickr.com/photos/lotus-salvinia. (J) Tendrils derived from the modified inflorescence tip in Antigonon leptopus (Polygonaceae). (K) Tendrils are modified pedicels in Antirrhinum filipes (Plantaginaceae). Arrows indicate tendrils.

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