Systematic treatment of morphological fruit types in plants of the class Liliopsida of the flora of Ukraine

In this review, the scope of morphological diversity of fruits within the class Liliopsida belonging to the flora of Ukraine compared to the world flora diversity was analyzed. For the first time, the taxonomic diversity of monocot plants of the flora of Ukraine was analyzed, which includes 235 genera and about 1050 species, and the distribution of fruit types in the largest monocot families revealed. It was found that among monocot plants of the world flora, as also of the Ukrainian flora, more than 70% of generic and species diversity is taken up by the Orchidaceae, Poaceae, and Cyperaceae families having dry uniform fruits: inferior capsule (Orchidaceae) and one-seeded enveloped fruit (Poaceae and Cyperaceae). An annotated list of morphological fruit types was compiled for all 38 families of the natural and cultural flora of monocot plants of Ukraine. Among 12 families of the subclass Alismatidae, apocarpous polymerous or trimerous fruits, mostly with one-seeded fruitlets, occur in six families (Alismataceae, Butomaceae, Potamogetonaceae, Ruppiaceae, Scheuchzeriaceae, Zannichelliaceae). In 12 of 16 families of the subclass Liliidae, trimerous capsules are the most common (Agapanthaceae, Agavaceae, Alliaceae, Amaryllidaceae, Asphodelaceae, Colchicaceae, Hemerocallidacae, Hyacinthaceae, Iridaceae, Liliасеае, Melanthiaceae, Orchidaceae), while in six families berry-like fruit occurs in all members or in the single genus (Asparagaceae, Ruscaceae, Dioscoreaceae, Melanthiaceae (Paris), Liliасеае (Streptopus), Smilacaceae). Among 10 families of the subclass Commelinidae, in four families superior dry one-seeded fruits occur (Cyperaceae, Poaceae, Sparganiaceae, Typhaceae), while another four families have trimerous capsules (Cannaceae, Commelinaceae, Juncaceae, Pontederiaceae). In general, the most typical fruit on the familial taxonomical level is the capsule (17 families), berries occur in 10 families, aggregate fruits and one-seeded fruits are represented each in seven families, while the rarest fruit type is the schizocarp (Juncaginaceae). No monomerous follicles, poricide and operculate capsules, winged fruits and loments were found. The most controversial fruit types are found in two groups of families, for both of them the problem is the gynoecium type. These are families with one-seeded fruit (Аrасеае (Lemna), Cyperaceae, Hydrocharitaceae (Najas), Poaceae, Sparganiaceae, Typhaceae, Zosteraceae) and families with initial carpel fusion (Hydrocharitaceae (Stratiotes), Juncaginaceae, Melanthiaceae (Veratrum), Scheuchzeriaceae, Tofieldiaceae). As a result of our work, the key and the most relevant areas of carpological studies in Ukraine were defined, particularly, unifying the terminology, examination of the anatomical structure of the pericarp, revealing of the evolutionary and ecological aspects of fruit morphology.


Introduction
Fruit is defined as a terminal stage of differentiation and specialization of the gynoecium together with persistent floral parts (Teryokhin, 2000). Although fruit characters are widely used in systematics (Cronquist, 1981;Takhtajan, 1987Takhtajan, , 2009, this happens substantially less often than usage of the flower characters. This is due to the fact that fruit structure often undergoes parallel evolution and convergence in many clades, which makes it difficult to use carpological data in evolutionary morphology and systematics. It was stated that fruit are too versatile and have too many aspects to be divided into strict categories (Pijl, 1982). However, morpho-anatomical fruit structure is a combination of many apomorphic characters of plant species, related to their reproductive system, which emphasized the need to reveal homologous fruit features in different species and identify trends of fruit evolution ). Such examinations are not possible without an unequivocal and adequate terminology on fruit structure and typology.
In Ukraine research on fruit structure began in the 1980s and has been carried out mainly in the relation to the systematics of defined families or plant introduction (Ziman & Bulakh, 2013). Predominantly, anatomical features and ultrastructure of fruit surface were studied, as also taxonomically significant morphological fruit traits. The latest monograph studies on fruit in plants of the flora of Ukraine were carried out on the genus Campanula (Dremliuga, 2013) and the Brassicaceae family (Ilyinska, 2016). However, generalized researches on morphological diversity and classification of fruits were absent. The necessity of such research is obvious to plant taxonomists, phytocoenologists, and ecologists using data on fruit adaptive and evolutionary-marker features in their studies. In this relation, in our neighbouring states structural carpological studies are actively proceeding in the XXI century, for instance, Slovakian botanists have published an atlas of seed and fruit morphology with descriptions of seeds and indehiscent fruits of 4,800 species (Bojňanský & Fargašová, 2007); in Poland, a bibliography of carpological works was published with more than 140 cited sources from Polish botanists (Latowski et al., 2015). Russian botanists are developing a morphogenetic approach and study of pericarp anatomy Kravtsova, 2015;Bobrov & Romanov, 2019).
The problem of fruit classification and evolution is closely related to the problems of the classification and evolution of the gynoecium, a structure bearing many adaptive and evolutionary significant fruit traits. In this article, we intend to analyze the known data on morphological fruit diversity within monocotyledonous plants, to compile fruit names applied to one taxon in home and foreign literature, to evaluate the occurrence of diverse morphological fruit types of the flora of Ukraine within the class Liliopsida Batsch, to reveal the most common fruit types, as also families of the flora of Ukraine having the most controversial fruit types with a view to their further investigation.

Taxonomical diversity of the class Liliopsida in the flora of Ukraine and main fruit types
The class Liliopsida in the world flora comprises 78 families, 2612 genera, and from 56 310 (Thorne & Reveal, 2007) to 60 100 species (www.mobot.org/MOBOT/research/APweb). Monocotyledonous plants of the flora of Ukraine encompass 38 families, recognized by Mosyakin (2013) or 30 families sensu Chase et al. (2016), which is about 40% of the world monocot familial diversity. The extent of the class Liliopsida belonging to the flora of Ukraine was defined including the cultivated taxa, as stated in the work of Mosyakin (2013). According to the published data (Mosyakin & Fedoronchuk, 1999), the monocot flora of Ukraine includes 235 genera and about 1050 species, which is less than 10% of genera and only about 1.5% of species of the world monocot flora. Taxonomical diversity of Liliopsida is five times less than dicotyledonous diversity (Thorne & Reveal, 2007), for this reason, we may expect a less expressed structural diversity of fruits within Liliopsida compared to the general diversity of angiosperm fruits. Within the class Liliopsida of the world flora, the first places in species richness are occupied by the families Orchidaceae, Poaceae, and Cyperaceae, embracing in total 74% of species and 70% of generic monocot richness. These families are characterized by uniform dry fruits: inferior capsule (Orchidaceae) and one-seeded enveloped fruits (Poaceae and Cyperaceae, Table 1). This fact results in the quantitative prevalence of corresponding fruit types in the class Liliopsida and even further restricts the limits of expected fruit diversity in the rest of the monocot taxa. Among the largest monocot families of the world flora, dry capsular fruits prevail, being the dominant or the most common fruit type in six of ten families. Within the top listed families, one-seeded fruits occur in addition to Poaceae and Cyperaceae also in Arecaceae and Araceae (in particular, Lemnaceae, included in Araceae). Berry-like fruits occur in some Asparagaceae, Araceae and Bromeliaceae (Table 1).
Within the class Liliopsida of the flora of Ukraine, the first places in species richness are occupied by seven of ten largest monocot families of the world flora, which means high representation of monocot plants of the flora of Ukraine on the familial level. The richest monocot families in the flora of Ukraine in terms of species diversity are the same three families as of the world flora, embracing totally 70-77% monocot species of the flora of Ukraine. Among the ten largest monocot families of the flora of Ukraine, capsular fruits are also found in six families (Table 1).

Table 1
Fruit types in the ten largest monocot families of the world flora and flora of Ukraine  Chase et al. (2016); for the flora of Ukraine, families recognized by Mosyakin (2013) are noted; the number of genera and species in the world flora given after www.mobot.org/MOBOT/research/APweb, in the flora of Ukraine -after Mosyakin & Fedoronchuk (1999) and Danylyk (2012) for Cyperaceae.
The survey of the published data on fruit diversity in monocots is complicated by the application of molecular genetic methods in taxonomy during the last two decades, which has substantially changed the system of the class Liliopsida. These methods have revealled substantial differences between traditional evolutionary systems of the end of the XX century and the new scenario of clade phylogenesis (Chase, 2004;Thorne & Reveal, 2007;Mosyakin, 2013;Chase et al., 2016). As a result, the extent of subclasses, some orders and families was changed; especially it concerns the families of the order Asparagales (Mosyakin & Buyun, 2013). In this relation, it is desirable to analyze the fruit traits as potential synapomorphies of newly recognized clades as also to retain their representation in the flora of Ukraine.

Characteristics of main fruit types in the monocots
The names of fruit types are given based on different principles of fruit classification (Kaden, 1965;Roth, 1977;Artjuschenko & Theodorov, 1986;Levina, 1987;Spjut, 1994;Bobrov et al., 2009;Bobrov & Romanov, 2019). The lack of a formalized terminology in the carpological literature causes many difficulties during the analysis of multisource data for one taxon, and during comparison of data for several taxa. For instance, the phrases: "capsule inferior syncarpous dorsiventral" (Kaden, 1965), "capsule dehiscent by valves" (Тakhtajan, 1985), and "capsule loculicidal" , given for Iridaceae, have the same meaning.
To make possible the treatment of published data on the distribution of fruit types inside the class Liliopsida of the flora of Ukraine, we compiled an annotated list of names of fruit types, used in specialized home and foreign literature. This list has shown a range of diversity of fruit types in each family and the diversity of names given for fruit in each taxon. We did not examine in detail the morphogenetic Bobrov & Romanov, 2019) and carpological (Spjut, 1994) approaches to fruit classification because these concepts need a special discussion, however, some data cited from those works for some taxa are taken without discussion. We distributed fruit names in the annotated list according to descriptive and comparative-morphological principles (Artjuschenko & Theodorov, 1986;Levina, 1987;Bobrov et al., 2009) into five principal fruit categories, given below. Then, we treated these categories in monocot subclasses and families.
Schizocarp (ukr. skhizokarpiy, drobnyi plid) -syncarpous low-seeded fruit splitting longitudinally into a few unicarpellate units (mericarps). Such fruit is considered to be derived from capsular fruit or pyrenarium, having an advantage in that seeds are dispersed with pericarp covering.
One-seeded fruit -unilocular fruit developed from the monomerous or pseudomonomerous gynoecium, bearing only one seed, as a rule indehiscent, with various pericarp consistency. It is the most difficult fruit type for interpretation because it is the result of reduction in the number of carpel and seeds in the apocarpous or syncarpous gynoecium. This category embraces fruits, called achene, cypsela (ukr. sim'yanka), nutlet (ukr. horishok), nut (ukr. horikh), caryopsis (ukr. zernivka), utricle (ukr. mishechok), and drupe (ukr. kistyanka). Drupaceous fruit or drupe (ukr. kistyanka), is characterized by strong differentiation of the inner mechanical zone of the pericarp, forming a stone (putamen). It is as a rule an indehiscent one-seeded fruit or fruitlet. Syncarpous drupe is called pyrenarium. Because a drupe is reliably recognized only by the anatomical study of the pericarp, which is not always taken into consideration in taxonomical works, we classified multi-drupe as an aggregate fruit and uni-drupe and pyrenarium as one-seeded fruit.

Annotated list of morphological fruit types of monocot plants of the flora of Ukraine
In this list, for all monocot families of the flora of Ukraine, the descriptive and morphological fruit traits were outlined, as also ovary insertion (superior or inferior), seed number, placentation, presence of envelope, and mode of dehiscence, if such information is known from published sources. Fruit types are presented only for genera occurring in the flora of Ukraine. Families are listed alphabetically and distributed in subclasses Alismatidae, Liliidae, and Commelinidae within the framework of Mosyakin (2013), where authors of names of taxa are given. Asterisked (*) are the families of cultural flora or those which have escaped to the wild. Alternative data for one taxon are separated by a semicolon (;). We submitted only basic sources for each family, since the informational pool for some taxa substantially exceeds the volume of a journal article.

Distribution of the main morphological fruit types in monocot subclasses and families
As a result of the treatment of the published data, we revealed apocarpous polymerous or trimerous fruits (aggregate fruits) mostly with oneseeded fruitlets in six of twelve families of the subclass Alismatidae of the flora of Ukraine recognized by Mosyakin (2013). A few families have berry-like, one-seeded fruits, capsules, and schizocarp (Table 2). We did not consider as capsule some fruits in members of the Аrасеае and Hydrocharitaceae families, for which other fruit types were referred to in most later publications. Within 16 families of the subclass Liliidae trimerous capsules are the most common fruits in 12 families, in four families the fruit is berry-like, and two families with capsular fruit have berry-like fruits in the solitary genus (Streptopus in Liliaceae, Paris in Melanthiaceae). In some genera, deviations from trimerous groundplan occur (tetramerous fruit in Paris, dimerous fruit in Ruscus and Majanthemum of Ruscaceae). Within 10 families of the subclass Commelinidae, in four families superior dry one-seeded fruits occur (Cyperaceae, Poaceae, Sparganiaceae, Typhaceae), while another four families have trimerous capsule (Cannaceae, Commelinaceae, Juncaceae, Pontederiaceae). The families Arecaceae and Musaceae which are only cultivated in Ukraine possess drupaceous and berry-like fruits correspondingly. The most diverse subclass in terms of fruit morphology is Alismatidae, where all five main fruit types are revealed. In Commelinidae there are four main fruit types, while in Liliidae only two fruit types, capsule and berry, were revealed (Fig. 1).
Among families of the class Liliopsida of the flora of Ukraine, trimerous capsules are the most common type (17 of 38 families), occurring in all subclasses (Fig. 1). However, considering the great species richness of the Poaceae and Cyperaceae families, the most numerous fruit can be supposed to be one-seeded fruit, monocarpous or pseudomonocarpous, occurring in seven families. One-seeded fruitlets of aggregate fruits are also very common, particularly, in Alismataceae, Arecaceae, Potamoge-tonaceae, Ruppiaceae, Zannichelliaceae. Berries occur in 10 monocot families, however, these families are not large or there are solitary genera within families with capsular fruit. The rarest fruit type for monocot plants of Ukraine is schizocarp (Fig. 1), appearing only in one genus Triglochin (Juncaginaceae). Among the studied taxa there are no monomerous follicles, poricide and operculate capsules, winged fruits and loments revealed that occur in dicotyledonous plants (Levina, 1987). Most monocot families in the flora of Ukraine are homogenous in carpological traits. This presumably results from the fact that few taxa represent many monocot families in the flora of Ukraine. However, in six families several fruit types were revealed (Alismataceae, Araceae, Arecaceae, Hydrocharitaceae, Liliaceae, Melanthiaceae).  Many monocot families have unambiguously defined fruit types, which however can differ in minor traits according to different sources. For example, the different definitions can concern the dehiscence mode of the capsule or pericarp consistency. Most of these families (15 of 27 families) belong to the subclass Liliidae and have trimerous capsular or berrylike fruits. For 11 families (29% of families), two or more interpretations of morphological fruit type exist. Among them, one case is a group of families with initial carpel fusion (Hydrocharitaceae (Stratiotes), Juncaginaceae, Melanthiaceae (Veratrum), Scheuchzeriaceae, Tofieldiaceae), resulting in fruit type being formed of a transitional stage between apocarpous and syncarpous and that is why it is defined as multi-follicle (apocarpous fruit) or capsule and schizocarp (syncarpous fruit). The other group of families unites families with one-seeded fruit, being treated as monomerrous apocarpium or pseudomonocarpium because of the absence of transitional stages between one-seeded and ancestral fruit (Аrасеае (Lemna), Cyperaceae, Hydrocharitaceae (Najas), Poaceae, Sparganiaceae, Typhaceae, Zosteraceae). In both cases, the reason for the controversial interpretation of the fruit type concerns gynoecium structure, which is still problematic (Remizowa et al., 2006(Remizowa et al., , 2010Sokoloff, 2016;Sokoloff et al., 2017). It is interesting that the Hydrocharitaceae family appears in both lists of controversial fruit types, and fruit in Stratiotes is unique through the combination of almost unfused carpels and inferior ovary (Efremov et al., 2015а). The examination of gynoecium structure and pericarp anatomy in various monocot plants of the flora of Ukraine is a ground for future research on evolutionary fruit morphology and fruit adaptations to dissemination.

Conclusions
As a result of our study, it becomes clear that the taxonomical diversity of monocotyledonous plants of the flora of Ukraine represents well the diversity of the world monocot flora, with an almost equally high portion of the largest families that define the spectrum of fruit types in the class Liliopsida. The morphological diversity of fruits within the class Liliopsida in the flora of Ukraine is characterized by the predominance of trimerous capsules on the familial level and one-seeded fruits and fruitlets on the generic level. Fruits in many families have alternative names due to the lack of unified carpological terminology, different degrees of knowledge of the fruit structure and different opinions on the gynoecium and fruit classification in taxa that are problematic from the morphological viewpoints. The most controversial fruit types are in plants with one-seeded fruit (monocarpium or pseudomonocarpium). The problem also arises for the definition of fruit type in plants with initial carpel fusion. The great number of families with trimerous capsules led to the need to apply anatomical methods in the study of pericarp structure aimed at differentiating the convergent variants of fruits. Meanwhile, for the most problematic taxa, it is necessary to find principles of classification of the fruits with undefined gynoecium type. In general, the monocot plants of the flora of Ukraine are characterized by limited diversity of morphological fruit types and poor knowledge of the fruit structure, which makes further carpological studies in Ukraine a highly relevant topic for research. The present research was fully self-funded by the authors. No competing interests have been declared.