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Peristome Development Pattern in Encalypta Poses Arctoa (2018) 27: 1–17 doi: 10.15298/arctoa.27.01 PERISTOME DEVELOPMENT PATTERN IN ENCALYPTA POSES A PROBLEM: WHAT IS THE PRIMARY PERISTOMIAL LAYER IN MOSSES? ОСОБЕННОСТИ РАЗВИТИЯ ПЕРИСТОМА У ENCALYPTA ПОДНИМАЮТ ВОПРОС О ТОМ, ЧТО ЖЕ ТАКОЕ ПЕРВИЧНЫЙ ПЕРИСТОМНЫЙ СЛОЙ У МХОВ? MICHAEL S. IGNATOV1,2, ULYANA N. SPIRINA2,3, MARIA A. KOLESNIKOVA2, DARYA A. ASHIKHMINA1, ELENA A. IGNATOVA1 & SVETLANA V. P OLEVOVA1 МИХАИЛ С. ИГНАТОВ1,2, УЛЬЯНА Н. СПИРИНА2,3, МАРИЯ А. КОЛЕСНИКОВА2, ДАРЬЯ А. АШИХМИНА1, ЕЛЕНА А. ИГНАТОВА1, СВЕТЛАНА В. ПОЛЕВОВА1 Abstract Peristome development was studied in mosses of the subclass Funariidae: Encalypta procera, E. longicolla, E. rhaptocarpa, E. vulgaris, Timmia bavarica and Funaria arctica. Peristome of Encalyptaceae is characterized by thick inner peristomial layer (IPL), so up to the late stages of its development its cells do not divide, maintaining basic peristomial formula 4:2:2 (omitting preperistomial layers). No regular offsetting is seen, and cells in all amphithecial layers are aligned by their anticlinal cell walls. Further development to the stage of 4:2:4 may proceed very late, so the formula 4:2:2 may remain in mature peristomes. Moreover, occasional anticlinal divisions occur in primary peristomial layer (PPL), so one IPL cell sometimes adjoins to two cells in the PPL. Such anticlinal divisions in PPL are also observed in Timmia, though we failed to find them in Funaria. The revealed additional divi- sions in PPL pose a question on its definition. Original criteria for PPL recognition given by Blomquist & Robertson (1941) are discussed and found contradicting the pattern in Encalypta in a number of important aspects. In all studied species of Encalypta the IPL seems to keep a development regulatory functions, which are a characteristics of PPL in peristomes of most arthrodontous mosses. This devel- opmental pattern of peristome in Encalypta may explain an extraordinal diversity of peristomes in this genus, varying from 5-layered to simple and then to totally reduced. Neglected aspects of the peristome development in Funaria are also discussed. Резюме Изучено развитие перистома у мхов подкласса Funariidae: Encalypta procera, E. longicolla, E. rhaptocarpa, E. vulgaris, Timmia bavarica и Funaria arctica. Перистомы Encalyptaceae характе- ризуются сильным утолщением клеток внутреннего перистомного слоя (ВПС), и в процессе их развития долгое время расположение клеток в перистомных слоях соответствует базовой перистом- ной формуле 4:2:2 (не принимая во внимание предперистомные слои). Смещения клеток в пери- стомных слоях не наблюдается, и периклинальные стенки всех перистомных слоев остаются выровненными относительно друг друга. Переход к следующей стадии развития, которой соот- ветствует перистомная формула 4:2:4, может происходить очень поздно, или формула 4:2:2 мо- жет сохраняться в зрелых перистомах. Более того, в клетках первичного перистомного слоя (ВПС) иногда происходят антиклинальные деления, и в таких случаях к одной клетке ВПС будут примы- кать две клетки первичного перистомного слоя (ППС). Такие антиклинальные деления в ППС также происходят у Timmia, однако мы не нашли их у Funaria. Выявленные дополнительные деления в ППС ставят вопрос о том, что такое первичный перистомный слой. Обсуждаются критерии, изначально предложенные Бломквистом и Робертсоном (Blomquist & Robertson, 1941) для различения ППС; показано, что многие важные признаки ППС отсутствуют у перистомов Encalypta. По-видимому, у всех изученных видов Encalypta ВПС играет основную роль в регуляции развития перистома, которая обычно приписывается ППС у большинства мхов с артродонтным перистомом. Эта особенность развития перистома у Encalypta может служить объяснением экстра- ординарного разнообразия перистомов у видов этого рода, которые варьируют от пятислойных до полностью редуцированных. Обсуждаются также некоторые аспекты развития перистома Funaria, которым ранее не уделялось внимание. KEYWORDS: bryophytes, evolution, haplolepideous, arthrodontous, sporophyte 1 – Faculty of Biology, Moscow State University, Moscow 119991 Russia; e-mail: [email protected], [email protected], [email protected] 2 – Tsitsin Main Botanical Garden of Russian Academy of Sciences, Botanicheskaya 4, Moscow 127276 Russia; e-mail: [email protected] 3 – Faculty of Biology, Tver State University, Zhelyabova 33, Tver 170100 Russia; e-mail: [email protected] 2 M.S. IGNATOV, U.N. SPIRINA, M.A. KOLESNIKOVA, D.A. ASHIKHMINA, E.A. IGNATOVA, S.V. POLEVOVA INTRODUCTION logenetic significance, maybe comprising an early stag- Peristome is a structure for controlling spore discharg- es of transition to the haplolepideous mosses. ing in mosses, and therefore it is of crucial importance Consequently the discussion on the peristome of En- for their life. In most groups of mosses, peristome is com- calypta by Edwards (1979, 1984) and Horton (1982) con- posed of either one circle of 16 elements, called teeth, or tributed much to understanding of the Encalyptaceae mor- of two circles of 16 elements each. These elements are phology and evolution. However, the developmental as- usually developed from three concentric layers of cells, pects were still scarcely observed, so we decided to per- which are largely decomposing, excepting tangental cell form this study for better understanging of peristome walls adjoining in a specific ways, so the inner cell wall structure in the Encalyptaceae and reasons for its great of the outer peristomial layer adjoins to the outer cell variation. wall of the middle cells layer, while the inner cell wall of MATERIAL AND METHODS this middle layer adjoins to the outer cell wall of inner Sampling. Although the molecular phylogenetic stud- peristomial layer (Edwards, 1979, 1984; Shaw & Robin- ies never adressed Encalypta specifically, a rather broad son, 1984; Shaw & Renzaglia, 2004; Shaw et al., 2011). selection of its species was represented in a number of An outstanding regularity in cell divisions in the de- broaded phylogenies (Tsubota et al., 2004; Ignatov et al., veloping capsule has been already observed by Kienitz- 2016), which confirms the general system of the genus Gerloff (1878); then Evans and Hooker (1913) counted worked out already by Philibert (1889), Brotherus (1924), number of cells in the developing peristome and found a and Horton (1982, 1983). Four species of Encalypta were fixed number of cells in two concentric layers which pro- selected for this study in order to include both basal and duce peristome in Ceratodon. teminal representatives of the genus: E. procera, one of Homology and terminology of peristomial layers were the basalmost species in the molecular phylogenetic trees developed by Blomquist & Robertson (1941) and Kreulen (Tsubota et al., 2004); E. longicollis, another species from (1972), and Edwards (1979) introduced peristomial for- the basal grade, with the “secondary nematodontous” mulae, which present the proportion of cells in three (or peristome formed by 4-5 cell layers; E. rhaptocarpa, a more) peristomial layers. Subsequent studies revealed not representative of the terminal clade, with a well devel- only usefulness of the peristomial formulae, which spread oped endostome and exostome only a little shorter and over handbooks, but also it was found that they nicely adhaerent to endostome; and E. vulgaris, a species closely correlate with the main phylogenetic moss lineages (New- related to the previous one, but eperistomate. Two other ton et al., 2000; Shaw et al., 2011; Frey & Stech, 2009; mosses of the subclass Funariidae, or ‘diplolepideous Goffinet et al., 2009). In Fig. 1 this principal scheme is opposite’, Funaria arctica and Timmia bavarica were summarized in accordance with current knowledge. This taken for comparison, in order to have comparable im- general rule of peristome evolution provided a possibili- ages using the same methods and based on the material ty to evaluate specific exceptional cases, such as Ca- collected at similar stages of development. toscopium (Ignatov et al., 2015) and Pseudoditrichum The material was collected when setae reached one (Fedosov et al., 2016). third of their full length, but the capsule itself did not Representatives of most moss orders were already start to become broader than the seta. As sporophyte de- studied for the peristome development, although the velompent proceeds acropetally, the earliest stages of Encalyptales were not specially addressed in this respect peristome development were seen in its distal parts, while up to now. At the same time, peristomes of Encalyptaceae below the later stages were available. As we mostly did attracted attention in the first bryological studies in 18th not trace all stages for each individual species, the struc- century (see review of Horton, 1982). The fact that such ture of IPL (where divisions are commonly delayed in small genus has so diverse peristome structure was not- Enclaypta) was observed under SEM, by observations ed already by Nees et al. (1827), and a rather modern on peristome surface from inside. species grouping in the genus is dated by the second edi- Preparation and Microscopy. All material was col- tion of Synopsis Muscorum Europaeorum’ (Schimper, lected in the field, fixed shortly after collecting in 2.5% 1876). The important step forward was done by Philibert glutaraldehyde in 0.05M PBS. Further steps vere done (1889, revised and abridged in English by Taylor, 1962), after several weeks or few months. Specimens were post- who noticed the similarity of peristomes of E. longicollis
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