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Periodization in the Development of Flowering Plant Reproductive Structures: Critical Periods

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Periodization in the Development of Flowering Plant Reproductive Structures: Critical Periods ACTA BIOLOGICA CRACOVIENSIA Series Botanica 45/1: 27–36, 2003 PERIODIZATION IN THE DEVELOPMENT OF FLOWERING PLANT REPRODUCTIVE STRUCTURES: CRITICAL PERIODS TATYANA B. BATYGINA* AND VALENTINA E. VASILYEVA Department of Embryology and Reproductive Biology, Komarov Botanical Institute, Prof. Popov Str. 2, 197376 St. Petersburg, Russia Received August 12, 2002; revision accepted February 27, 2003 The theory of critical periods in plant ontogenesis has been elaborated from studies of integral morphogenetic processes on different levels. The periodization of the development of various reproductive structures (anther, microspore, pollen grain, ovule, megagametophyte, egg cell, zygote and embryo) has been worked out from data on morphogenesis using systemic and complex morphophysiological approaches. Critical phases, stages and periods have been revealed, for example the stage of autonomy in different flowering plants, by means of culture in vitro. The concepts of "critical period" and "critical mass" in relation to embryonal structure periodization are discussed here. Also addressed are the question of allometry and the significance of morphogenetic fields and rhythms of cell division for revealing critical periods and the management of ontogenesis. Examination of the genesis and structure of anthers and ovules in various flowering plant species has permitted us to discover general regularities in their development and the occurrence of three common critical periods: premeiotic, meiotic and postmeiotic. Embryo development in angiosperms is characterized by two common phases (proem- bryonal/blastomerization and embryonal/organogenesis) and five critical periods (zygote and proembryo, globular, heart-shaped, torpedo-shaped, and mature embryo). The combination of common and specific critical periods and stages determines the taxon-specific morphogenesis of reproductive structures and contributes to the plasticity and tolerance of the reproductive systems of different species of flowering plants, and of ontogenesis as a whole. Key words: Critical period, critical mass, morphogenetic fields, reproductive structures, switching over development program. INTRODUCTION zygote and embryo – and put forward a strategy for studying reproductive structure: (1) investigation of Elaborating the theory of critical periods, stages the dynamics of anther, ovule and seed structures and phases during ontogenesis is an important and their interrelation with the surrounding tis- problem in biology. The information gained sues; (2) comparison of the kinetics of morphogenetic through investigation of the integral events in the and physiological biochemical processes; (3) com- morphogenesis of reproductive organs in flower- parison of the regularities of anther, ovule and em- ing plants and the changing pattern of their spa- bryo differentiation in situ, in vivo and in vitro; and tial organization offers the possibility of control- (4) choice of model plant species, contrasted by their ling individual development (Stockard, 1921; embryological features, ecotype and ecology, and Svetlov, 1960; Tokin, 1987). We have suggested etiology of germination in relation to the plant’s the periodization of the development of the basic position in the phylogenetic system of angiosperms reproductive structures – anther, ovule, egg cell, (Batygina et al., 1992). *e-mail: [email protected] PL ISSN 0001-5296 © Polish Academy of Sciences, Cracow 2003 28 Batygina and Vasilyeva Fig. 1. Critical mass formation during morphogenesis in situ and in vitro. (a) Mature zygote transition to division, (b) Transition from globular stage of embryo development to embryoderm formation, (c) Transition to heart-shaped stage of embryo development (after Batygina, 1984), (d) Influence of the density of the population on embryoid differentiation and their viability in cell culture of carrot (after Halperin, 1967, modified). CRITICAL CELLULAR MASS cell suspension, the correlation between the degree AND MORPHOGENETIC FIELDS of differentiation of embryoids, their survival, and IN THE REPRODUCTIVE SYSTEM the degree of inoculate dilution (Halperin, 1967), that is, the critical mass of cells, was established The totipotency of the plant cell defines the continu- (Fig. 1). ation of morphogenesis throughout ontogenesis. The For plant reproductive structures, the origin of whole of ontogenesis could be determined as a par- all cells and their relationship can be revealed at ticular function of meristem growth to a certain early stages. At later developmental stages the role critical mass (Fig. 1). We understand critical cellular of each single cell in the system decreases. However, mass as the minimum number of cells or the mass intercellular cooperation significantly increases and of a single cell required for morphogenesis of any morphogenetic fields are formed (Batygina, 2000). structure, or in other words "not more than is abso- From the standpoint of modern ideas and facts (Gil- lutely needed" in accord with the embryogenetic law bert et al., 1996), the concept of "morphogenetic of economy (Johansen, 1950). For example, at a field" acquires a new significance when one exam- definite critical stage of embryo development, dif- ines the periodization of reproductive structures. We ferentiation of protoderm, conditioned by the ap- refer to the morphogenetic field as a definite mor- pearance of embryo critical mass, takes place phogenetic zone in which the pattern of cell division simultaneously with the beginning of exponential and the direction of growth is strictly determined, growth (Batygina, 1984a; Vallade, 1989). In carrot and in which these cells occupy positions corre- Periodization and reproductive structure development 29 sponding to their roles in this system (in agreement ontogenesis, a transitive critical period between spo- with the law of disposal, Souèges, 1937). Each rophytic and gametophytic generations. In the clas- species is characterized by a definite number of sic understanding, meiosis is completed with the critical masses and morphogenetic fields. Differen- formation of micro- and megaspore tetrads. How- tiation of the reproductive structures and the entire ever, some embryological data (on the development organism may be accompanied by the formation of of embryo sacs of different types) suggest that the several critical masses, which determine the "thresh- meiotic period can finish later, namely after disinte- old of factors" required for establishing any morpho- gration and specialization; that is, it draws in the genetic pathway (embryogenesis, embryoidogen- whole process of micro- and megasporogenesis. esis, organogenesis and histogenesis) both in situ Microspores represent the initial cells of gameto- and in vitro. phyte generation. The formation of the gametophyte proper provisionally begins in the postmeiotic period with microspore germination – its division. The oc- CRITICAL PERIODS, CRITICAL STAGES currence of enormous abnormalities during micro- IN REPRODUCTIVE STRUCTURE and megaspore development confirms our sugges- DEVELOPMENT tion. It should be emphasized that the division of the developmental process into premeiotic, meiotic and Earlier investigators examined the "critical period", postmeiotic periods is rather a conditional one, as the "critical stage" ("transitional moment") as the meiosis itself is a highly plastic process and cannot stage of ontogenesis in which the structures display coincide precisely with the stages of micro- and the greatest sensitivity to unfavorable environmen- megasporogenesis; moreover, meiosis I is sometimes tal factors. We interpret the critical period more absent (in the case of diplospory). loosely as including a number of stages. Our basis The premeiotic period in anther development for distinguishing critical moments consists in the includes three critical stages: (1) differentiation of morphogenetic and morpho-physiological correla- certain cells of the anther primordium to archespo- tions that cause allometries of the reproductive rium; (2) division of archesporial cells into sporogen- structures at different developmental stages and ous tissue and parietal layer; and (3) determination their architecture. In investigating the critical peri- of a centripetal pattern of anther wall development. ods and stages, we observed the specific and nonspe- The meiotic period is characterized by the transi- cific reactions of the plant to one or another source tion from diplophase to haplophase and includes two of influence. Comparative analysis of data on the critical stages: (1) initiation of meiosis in the microspore genesis of anthers and ovules in various flowering mother cells, formation of callose, formation of micro- plant species permitted us to outline the periodiza- spore tetrads; and (2) development of the microspore.* tion of their development and discover common (pre- The postmeiotic period (formation of the ga- meiotic, meiotic, postmeiotic) and specific critical metophyte proper) includes three critical stages: (1) periods and stages. microspore "germination" and unequal microspore division, yielding the generative and vegetative CRITICAL PERIODS AND STAGES cells, together making up the pollen grain; (2) dis- IN ANTHER DEVELOPMENT placement of the generative cell and vegetative cell nucleus in the pollen grain; and (3) gametogenesis. Anther development in cereals offers an illustration The postmeiotic period is associated with matura- of the critical periods (premeiotic, meiotic, post- tion and developmental disintegration
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