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Reproductive Development and Genetic Structure of the Mycoheterotrophic Orchid Pogoniopsis Schenckii Cogn

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Reproductive Development and Genetic Structure of the Mycoheterotrophic Orchid Pogoniopsis Schenckii Cogn Alves et al. BMC Plant Biol (2021) 21:332 https://doi.org/10.1186/s12870-021-03118-y RESEARCH Open Access Reproductive development and genetic structure of the mycoheterotrophic orchid Pogoniopsis schenckii Cogn. Mariana Ferreira Alves1*, Fabio Pinheiro1, Carlos Eduardo Pereira Nunes1, Francisco Prosdocimi2, Deise Schroder Sarzi2, Carolina Furtado3 and Juliana Lischka Sampaio Mayer1 Abstract Background: Pogoniopsis schenckii Cogn. is a mycoheterotrophic orchid that can be used as a model to understand the infuence of mycoheterotrophy at diferent stages of the reproductive cycle. We aimed to verify the presence of endophytic and epiphytic fungi at each stage of the reproductive process and investigated how the breeding system may relate to genetic structure and diversity of populations. In this study we performed anatomical and ultrastruc- tural analyses of the reproductive organs, feld tests to confrm the breeding system, and molecular analysis to assess genetic diversity and structure of populations. Results: During the development of the pollen grain, embryo sac and embryogenesis, no fungal infestation was observed. The presence of endophytic fungal hyphae was observed just within foral stems and indehiscent fruit. Beyond assuring the presence of fungus that promote seed germination, specifc fungi hyphae in the fruit may afect other process, such as fruit ripening. As other mycoheterotrophic orchids, P. schenckii is autogamous, which may explain the low genetic diversity and high genetic structure in populations. Conclusions: We discuss an interesting interaction: fungal hyphae in the indehiscent fruit. These fungal hyphae seem to play diferent roles inside fruit tissues, such as acting in the fruit maturation process and increasing the prox- imity between fungi and plant seeds even before dispersion occurs. As other mycoheterotrophic orchids, P. schenckii is autogamous, which may explain the low genetic diversity and high genetic structure in populations. Altogether, our fndings provide important novel information about the mechanisms shaping ecology and evolution of fragmented populations of mycoheterotrophic plant. Keywords: Autogamy, Embryology, Fungal hyphae, Genetic diversity, Mycoheterotrophy, Orchid Background for many years [2]. Mycoheterotrophy has independently Mycoheterotrophy is the parasitic relationship between evolved in several lineages, being reported in 10 angio- plants and fungi in which the plants depend on the inter- sperm families and approximately 515 species [3]. Tese action with fungi to fulfll part of their nutritional needs plants have lost their photosynthetic capacity and rely [1]. In presenting an unconventional way of life, mycohet- on carbon from associations with fungi throughout their erotrophic plants have been arousing botanical curiosity whole life cycle [2]. Due to their dependence on an obli- gate interaction, these species have a restricted distribu- *Correspondence: [email protected] tion, usually smaller than the distribution of the exploited 1 Departamento de Biologia Vegetal, Instituto de Biologia, Universidade fungi [4]. Tey are mostly found in low-light locations of Estadual de Campinas, São Paulo, Brazil underbrushes, where photosynthetic plants would be at a Full list of author information is available at the end of the article competitive disadvantage [1]. © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Alves et al. BMC Plant Biol (2021) 21:332 Page 2 of 14 Mycoheterotrophic plants exhibit numerous modif- consequences of mycoheterotrophy (but see [19, 24, 25]). cations. Tey are small, herbaceous, with reduced veg- Pogoniopsis is a Brazilian endemic genus composed of etative organs and, for most of their life cycle, remain two mycoheterotrophic species. Te reproductive data underground [2]. Infestations with fungi are not only for the genus show the absence of foral rewards and found in the roots, but also in underground organs such reproduction by autogamy [26], however, details of each as rhizomes and corms. Fungal infections in aerial organs reproductive stage and how this autogamy impacts the have not been described thus far, indicating that fungi genetic population diversity have not been investigated. propagation in the plant seems to be restricted to organs Another study reported the presence of fungi in the fo- close to the soil [2]. In seeds, infection generally occurs ral stem and fruits of P. schenckii Cogn. [27], difering in a short period after its germination, but in some cases, from what has been described for other species, where such as for mycoheterotrophic orchids, fungal infection the interaction only occurs underground [2]. In this study is mandatory for seed germination [1, 2, 5, 6]. Te frst conducted by Sisti et al. [27], the genera of fungi found studies on mycoheterotrophic species were focused on on the foral stem and fruits of the species were identi- the relationship between plant and fungi, though data on fed, nevertheless, the efects that this interaction has development, reproductive biology, genetics and ecology on the life cycle of the species was not evaluated. Tus, have drawn attention recently [1–3]. Pogoniopsis may be used as a model to understand struc- Due to high levels of specialization found in mycohet- tural, ecological and evolutionary consequences of myco- erotrophic species, most of which are related to reduc- heterotrophy on reproductive stages and dynamics of the tions in morphological traits [2] and genomes [7]; the species. Terefore, we answer the following questions: (a) association with fungal species is considered obligate. What is the structural pattern of fungal colonization of Accordingly, Bidartondo [1], proposed that it would be the fruits of P. schenckii? (b) Does interaction with fun- evolutionarily unstable for a mycoheterotrophic species gal hyphae occur during the anther, ovule and embryo already involved in an obligate symbiotic interaction to development? (c) Is autogamy the predominant breeding establish additional obligate associations. Tus, these system of this species, and to what extent limitations in species are expected to present reproductive strategies seed and pollen movement shape the genetic structure in that are less dependent on biotic vectors such as a gen- this rare and endemic orchid species? Finally, we discuss eralist pollination, spontaneous self-pollination and/or how fungal colonization may infuence the development allocation of resources for seed formation. of reproductive organs in this plant and how the breed- How mycoheterotrophy can impact the reproduc- ing system and pollination interactions may infuence the tion of these species is still a debatable issue. Autogamy genetic structure of this rare orchid. is, in fact, observed in many mycoheterotrophic plants [8–13]. However, species with mixed pollination sys- Results tems can be observed, such as those with self- and cross- Anther structure, microsporogenesis, microgametogenesis pollination mechanisms [14–17], but we can also fnd and germination of pollen grain completely xenogamous species, in which reproductive Pogoniopsis schenckii presents tetrasporangiate anther success depends on insect pollination [8]. Considering (Supplementary fle Fig. S1a). In the initial stages, the that mycoheterotrophy infuences the reproductive sys- anther primordium is composed of meristematic tissue. tem of species, we should also expect refections in the In young bud stamens, the anther wall is formed by epi- genetic structure of these populations. Indeed, genetic dermis, endothecium, middle layer, and tapetum, all uni- population studies revealed low levels of diversity and seriate. Te epidermis and endothecium are formed by interpopulation gene exchange in mycoheterotrophic periclinal fattened cells and remain intact throughout species, suggesting a prevalence of autogamy [18–22]. the development of the male gametophyte. Te middle Orchidaceae, one of the most diverse families of angi- layer has compressed cells that are reabsorbed through- osperms, accounts for about 235 mycoheterotrophic out development. Te tapetum is glandular and consists species [3]. Mycoheterotrophy has evolved indepen- of dense cytoplasm and evident nucleus cells. During the dently several times within the family [23], suggesting process of male gametophyte formation, tapetum cells convergent functional evolution, achieved through a are absorbed. widespread absence of morphological and physiologi- In the young anther, sporogenous
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