Morphological diversity and function of the stigma in Ficus species (Moraceae)

Abstract

The stigma plays several roles such as pollen hydration and selection, and pollen tube nutrition. In the Ficus-fig wasp mutualism, stigmata have an additional, almost unknown, function by representing a physical interface for both plant and wasp reproduction. We used light and electron microscopy to compare the detailed morphology of the stigmata of nine Ficus species of different sections and with different pollination modes and sexual expressions. Figs were collected at the stage when the stigmata were receptive for pollination. Stigmata in actively pollinated monoecious species have well developed papillae concentrated on the adaxial surface exposed towards the fig cavity. Conversely, the passively pollinated monoecious species have the whole surface of the stigmata covered by somewhat smaller papillae. In both actively and passively pollinated monoecious species these features are consistent, irrespective of style length. In all actively pollinated gynodioecious species, the stigmata of pistillate flowers were tubular or infundibuliform whereas in almost all actively pollinated monoecious species (except F. racemosa) the stigmata were filiform, with one branch or two asymmetric branches. In gynodioecious species the short-styled flowers in "male" figs show a limited receptive surface with small papillae, while the stigmata of long-styled flowers in "female" figs are covered by papillae that extend down the sides of the style, increasing the stigmatic surface. In actively pollinated species, stigmata are cohesive, forming a common surface for pollen tube germination (= synstigma). The synstigma arrangement was quite variable: lax, cohesive or very cohesive, with entanglement by stigmatic papillae and stylar trichomes. Entanglement by stylar trichomes is common in gynodioecious species. The synstigma arrangement did not correlate with phylogeny or breeding system. This study is the first to report a very loose synstigma in actively pollinated monoecious Ficus species. Our analyses revealed that, in Ficus, the synstigma is functionally analogous to an extra-gynoecial compitum. Comparative studies will be required to test further hypotheses about the evolutionary determinants of such variation.

The synstigma turns the fig into a large flower

“…However, as of pollen tubes between the carpels. An extreme the synstigma of Ficus does not produce abundant case of this condition is the 'hyperstigma' described secretion (Heslop-Harrison & Shivanna, 1977;Ramírez-Benavides, 2007; present study), synstigma cohesion is mainly the result of the physical intertwining of the stigmatic branches and papillae (Teixeira et al, 2018). As such, the synstigma is functionally analogous to single flowers with carpels post-genitally and distally united, as found in Malvaceae, Apocynaceae and Sapindales Vieira & Shepherd, 2002).…”

“…The clade with the largest number of records so far is Ficus L. (Moraceae), with 500 species predicted to form synstigmas (Verkerke, 1989;Jousselin, Rasplus & Kjellberg, 2003b;Jousselin & Kjellberg, 2001;BassoAlves et al, 2014;Teixeira et al, 2018). A synstigma can be a continuous structure inside a syconium (the urn-shaped inflorescence of Ficus, the fig), composed of all stigmas of all flowers (Galil & Eisikowitch, 1968) or the result of contact between two or more stigmas of distinct flowers, acting as a common surface for pollen germination (Jousselin & Kjellberg, 2001;Jousselin Kjellberg & Herre, 2004, 2003a.…”

“…In passively pollinated species (those in which pollinating wasps have no behaviour of collecting/depositing pollen), the synstigma is not present and the flowers that receive the wasp eggs and the seed-producing flowers are morphologically different, especially regarding the length of the stigmas. The longer-styled flowers have long filiform stigmatic branches projecting into the fig cavity that brush the body of the wasp and collect pollen in the process, whereas the shorter-styled flowers have short filiform stigmatic branches stigmas that do not receive pollen (Jousselin et al, 2003a(Jousselin et al, , 2004Teixeira et al, 2018).…”

Fifty years later, figs and their associated communities

“…Initial descriptions of the stigmas as cohesive or non-cohesive were a caricature. New data on variation among fig species in stigma arrangement open up avenues for detailed behavioural investigations (Teixeira et al 2018). The high larval mortalities documented in two dioecious Ficus species (Ghana et al 2012) could be explained by imperfect correlation between oviposition into an ovule and actual pollination and fertilization of the ovule (Jousselin et al 2001).…”

Ficusplants: State of the art from a phytochemical, pharmacological, and toxicological perspective

“…The most Ficus plants are evergreen with a unique inflorescence, but in areas outside of the tropics these plants are deciduous. (Khadivi, Anjam, & Anjam, 2018; Ramirez‐Benavides, 2016; Teixeira, Costa, Basso‐Alves, Kjellberg, & Pereira, 2018). Berg (2003a, 2003b, 2003c, 2003d, 2004a, 2004b, 2006, 2007) distinguishes six subspecies in the Ficus genus: Ficus , Pharmacosycea , Sycidium , Sycomorus , Synoecia , and Urostigma .…”