Elucidating the evolutionary history of the Southeast Asian, holoparasitic, giant-flowered Rafflesiaceae: Pliocene vicariance, morphological convergence and character displacement

Bendiksby, Mika; Schumacher, Trond; Gussarova, Galina; Nais, Jamili; Mat-Salleh, K.; Sofiyanti, Nery; Madulid, Domingo A.; Smith, Stephen A.; Barkman, Todd J.

doi:10.1016/j.ympev.2010.08.005

Cited by 41 publications

(40 citation statements)

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“…Our results refute the simplistic scenario of floral evolution proposed for Rafflesiaceae, in which the floral chamber in Rafflesia and Sapria is thought to represent the ancestral condition within the family, which was then lost in Rhizanthes (15). Instead, our data suggest that the floral chambers in Rafflesia and Sapria are constructed differently and the involvement of the petal whorl is a Rafflesiaspecific invention.…”

Section: Discussionsupporting

confidence: 81%

“…Instead, our data suggest that the floral chambers in Rafflesia and Sapria are constructed differently and the involvement of the petal whorl is a Rafflesiaspecific invention. Given the evolutionary and phenotypic distance between Rafflesiaceae and its common ancestor with Euphorbiaceae (∼95 My) (15) and the widely accepted fact that parasitism can lead to drastic changes that confound assessment of homology (2,8,33), outgroup comparisons with Euphorbiaceae are problematic for understanding floral evolution in Rafflesiaceae.…”

Section: Discussionmentioning

confidence: 99%

“…This second model might seem unlikely, especially because the fly pollinators that visit these plants appear to be shared between the three Rafflesiaceae genera (13)(14)(15)(16). However, such changes are not without precedent and have been explained by developmental system drift (35).…”

Section: Discussionmentioning

confidence: 99%

“…1C), each with five similar lobes. Because of the striking similarity in floral morphology of these two genera, which represent the bulk of species diversity in the family, their floral chambers have been assumed to have originated once in the common ancestor of Rafflesiaceae (15) (Fig. 1).…”

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confidence: 99%

“…S1 G-K). Based on its more nested phylogenetic placement within the family, it has been assumed that the morphology of Rhizanthes is uniquely derived (15). The unusual floral organs of Significance Rafflesiaceae produce the world's largest flowers, but the developmental nature of their floral organs has remained a mystery.…”

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confidence: 99%

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Developmental origins of the world’s largest flowers, Rafflesiaceae

Nikolov

Endress

Sugumaran

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Rafflesiaceae, which produce the world's largest flowers, have captivated the attention of biologists for nearly two centuries. Despite their fame, however, the developmental nature of the floral organs in these giants has remained a mystery. Most members of the family have a large floral chamber defined by a diaphragm. The diaphragm encloses the reproductive organs where pollination by carrion flies occurs. In lieu of a functional genetic system to investigate floral development in these highly specialized holoparasites, we used comparative studies of structure, development, and gene-expression patterns to investigate the homology of their floral organs. Our results surprisingly demonstrate that the otherwise similar floral chambers in two Rafflesiaceae subclades, Rafflesia and Sapria, are constructed very differently. In Rafflesia, the diaphragm is derived from the petal whorl. In contrast, in Sapria it is derived from elaboration of a unique ring structure located between the perianth and the stamen whorl, which, although developed to varying degrees among the genera, appears to be a synapomorphy of the Rafflesiaceae. Thus, the characteristic features that define the floral chamber in these closely related genera are not homologous. These differences refute the prevailing hypothesis that similarities between Sapria and Rafflesia are ancestral in the family. Instead, our data indicate that Rafflesia-like and Sapria-like floral chambers represent two distinct derivations of this morphology. The developmental repatterning we identified in Rafflesia, in particular, may have provided architectural reinforcement, which permitted the explosive growth in floral diameter that has arisen secondarily within this subclade.ABC model | comparative gene expression | evo-devo | gigantism | parasitic plants

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Section: Discussionsupporting

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Developmental origins of the world’s largest flowers, Rafflesiaceae

Nikolov

Endress

Sugumaran

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Striking developmental convergence in angiosperm endoparasites

Teixeira‐Costa

Davis

Ceccantini

2021

American J of Botany

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Plant parasitism has evolved 12 times within flowering plants (Nickrent, 2020). This phylogenetic diversity is accompanied by a wide variety of habits, geographical distribution, host preferences, morphologies, and developmental patterns (Kuijt, 1969;Heide-Jørgensen, 2008). A broad spectrum of photosynthetic capabilities is also represented among these plants, ranging from species fully capable of photosynthesis, to those that are achlorophyllous during all or most of their life cycle, thus rendering them entirely reliant on host resources (Bromham et al., 2013). A subset of plants in the latter category exhibits a particularly extreme degree of reduction: their vegetative body is reduced to mycelium-like filaments of parenchyma cells embedded within their host tissues. In these cases, the parasite only becomes visible during reproduction when the flower/inflorescence temporarily emerges from its host (Mauseth, 1990;Meijer and Veldkamp, 1993;Nikolov et al., 2014b). Due to this extremely reduced growth form, restricted to life inside its host, these plants are commonly referred to as endoparasites.This highly modified and cryptic growth habit has been best described in detail from a small number of mistletoe species (Těšitel, 2016). Mistletoes are widely distributed parasitic plants known as keystone species in both natural and human-altered ecosystems (

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How many species of Rafflesia exist in Java, Indonesia and what are the implications for conservation?

Kusuma,

Matsuo,

Wanke

et al. 2023

Plants People Planet

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Societal Impact StatementClarifying species status for closely related taxa with similar and overlapping morphology is important for planning conservation efforts. Conservation of Rafflesia goes beyond merely saving species from extinction. It has far‐reaching societal impacts that touch on scientific discovery, cultural heritage, economic development, education, and more. Rafflesia interests many nature lovers, and so protected areas that preserve Rafflesia can become tourism hotspots, contributing to local economies and livelihoods. By conserving biodiversity, we acknowledge and value the interdependence of all living organisms, promoting a holistic understanding of nature. Biodiversity conservation is an investment in the health and well‐being of both ecosystems and human societies.Summary Species ambiguity could hinder conservation activities. Rafflesia is an endangered, holoparasitic, and endophytic plant genus that grows exclusively on Tetrastigma (Vitaceae) host plants. Overlapping morphological characters make their species delimitation difficult. Therefore, the number of Rafflesia species has been a major debate until now. On the island of Java, Indonesia, two or three species have been variously recognized. Here, we aim to illuminate the species status using single nucleotide polymorphisms (SNPs) marker obtained via a multiplexed ISSR genotyping by sequencing (MIG‐seq) approach. Clustering analysis with STRUCTURE indicates three different groups. Furthermore, the delimitation of the Javanese Rafflesia into three species is the favored model based on SNAPPER analysis. Phylogenetic analysis using Randomized Axelerated Maximum Likelihood (RAxML) also supports the distinction of the three groups. Although a SplitsTree4 analysis confirms the abovementioned results, it also highlights that Rafflesia patma shows broader gene flow compared to the other two species R. rochusenii and R. zollingeriana. We conclude that there are likely three species of Rafflesia on Java. Our study highlights the ability of using SNPs markers, in this case derived from a MIG‐seq approach, in approaching species uncertainty. The importance of clarifying the Rafflesia species status on Java Island for conservation planning is also discussed.

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Elucidating the evolutionary history of the Southeast Asian, holoparasitic, giant-flowered Rafflesiaceae: Pliocene vicariance, morphological convergence and character displacement

Cited by 41 publications

References 58 publications

Developmental origins of the world’s largest flowers, Rafflesiaceae

Developmental origins of the world’s largest flowers, Rafflesiaceae

Striking developmental convergence in angiosperm endoparasites

How many species of Rafflesia exist in Java, Indonesia and what are the implications for conservation?

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