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Phylogenetic Implications of Tetrasporangial Ultrastructure in Coralline Red Algae with Reference to Bossiella Orbigniana (Corallinales, Rhodophyta)

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Phylogenetic Implications of Tetrasporangial Ultrastructure in Coralline Red Algae with Reference to Bossiella Orbigniana (Corallinales, Rhodophyta) W&M ScholarWorks Dissertations, Theses, and Masters Projects Theses, Dissertations, & Master Projects 1933 Phylogenetic Implications of Tetrasporangial Ultrastructure in Coralline Red Algae with Reference to Bossiella orbigniana (Corallinales, Rhodophyta) Christina Wilson College of William & Mary - Arts & Sciences Follow this and additional works at: https://scholarworks.wm.edu/etd Part of the Biology Commons Recommended Citation Wilson, Christina, "Phylogenetic Implications of Tetrasporangial Ultrastructure in Coralline Red Algae with Reference to Bossiella orbigniana (Corallinales, Rhodophyta)" (1933). Dissertations, Theses, and Masters Projects. Paper 1539624407. https://dx.doi.org/doi:10.21220/s2-pbyj-r021 This Thesis is brought to you for free and open access by the Theses, Dissertations, & Master Projects at W&M ScholarWorks. It has been accepted for inclusion in Dissertations, Theses, and Masters Projects by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. PHYLOGENETIC IMPLICATIONS OF TETRASPORANGIAL ULTRASTRUCTURE IN CORALLINE RED ALGAE WITH REFERENCE TO BOSSIELLA ORBIGNIANA (CORALLINALES, RHODOPHYTA) A Thesis Presented to The Faculty of the Department of Biology The College of William and Mary in Virginia In Partial Fulfillment Of Requirements for the Degree of Master of Arts by Christina Wilson 1993 APPROVAL SHEET This Thesis is submitted in partial fulfillment of the requirements for the degree of Master of Arts Approved, July 1993 ph l / . Scott Sharon T . Broadwater Stanton F. Hoegerm DEDICATION For Sheila and Wesley Wilson iii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS................................. v LIST OF TABLES AND DIAGRAMS..................... vi LIST OF FIGURES.................................. vii ABSTRACT......................................... ix INTRODUCTION..................................... 2 MATERIALS AND METHODS.................. 9 RESULTS.......................................... 11 DISCUSSION 2 7 APPENDIX......................................... 48 BIBLIOGRAPHY..................................... 51 TABLES AND DIAGRAMS.............................. 56 KEY TO ABBREVIATIONS............................. 62 FIGURES.......................................... 63 VITA.................... 102 iv ACKNOWLEDGEMENTS The author wishes to acknowledge the following group of individuals for their special contributions to this study. Dr. Joseph L. Scott introduced me to the world of coralline red algae. As my primary mentor, he patiently guided me through the technical and theoretical aspects of the project. Dr. Sharon T. Broadwater and Dr. Stanton F. Hoegerman both played crucial roles in the preparation of the final manuscript. Finally, this study could not have been completed without the expert technical assistance of William Saunders and Jewel Thomas. v LIST OF TABLES AND DIAGRAMS FIGURE PAGE 1. Summary of coralline taxonomic schemes........ 56 2. Tetrasporogenesis in Bossiella orbiqniana 57 3. Survey summary................................ 58 4. Coralline classification sensu Cabioch........ 59 5. Coralline tetrasporangial nuclear development. 60 vi LIST OF FIGURES Figure Page 1. SEM of conceptacle-bearing intergenicula in Bossiella orbigniana............. 63 2-3. SEM of longitudinal sections through Bossiella tetrasporangial conceptacles.. 63 4. DAPI stained tetrasporocyte....... 64 5-6. DAPI stained stage 4 tetrasporangium.... 64 7. DAPI stained tetrasporangial conceptacle 65 8. Toluidine blue stained tetrasporangial conceptacle.......................... 65 9. DAPI stained stage 3 tetrasporangium..., 65 10. Toluidine blue stained stage 3 tetrasporangium...................... 65 11-13. PAS stained tetrasporangia............... 66 14-15. PAS/Toluidine blue stained tetrasporangium........................ 67 16-19. Early stage 1 tetrasporocyte........ 68 20-23. Stage 1 tetrasporocyte exhibiting elongation 6 9 24-30. Details of late stage 1 pre-meiotic tetrasporocytes...................... 70-71 31-32. Stage 2 meiotic nuclei............... 72 33-36. Details of early cleavage furrow formation during stage 2 ............ 73 37. Stage 3 vacuolate tetrasporangia..... 74 38-39. Localization of cleavage furrows-stage 3 74 vii 40-44. Stage 3 vacuolate nuclei ...............75-76 45. Starch-flanked stage 3 vacuoles....... - 76 46. Stage 3 chloroplast division.......... 76 47-49. Stage 3 mucilage secretion............. 77 50-56. Stage 3 post-vacuolate tetrasporangia... 78-81 57-68. Stage 3 post-vacuolate tetrasporangia showing EDM dispersal................... 82-84 69-77. Stage 4 fully cleaved tetrasporangia.... 85-87 78. Bisporangial conceptacle............... 88 79-82. Stage 3 vacuolate bisporangia......... 89 83-87. Stage 3 post-vacuolate bisporangia.... 90 88-89. Stage 4 bisporangial nucleus......... 91 90-92. Amphiroa............................. 92 93-95. Lithothrix............................. 93 96-97. Tit anode rma............................. 94 98-102. Fosliella............................... 95-102 103-105. Metamastophora................... 97 106-108. Haliptilon............................. 98 109-112. Jania................................. 99 113-116. Corallina.............................. 100 117. Calliarthron........................... 101 118. Bossiella.............................. 101 viii ABSTRACT The red algal order Corallinales is most commonly divided into seven subfamilies primarily on the basis of the presence or absence of genicula (articulations). This classification scheme has been criticized as phenetic rather than phylogenetic. Ultrastructural details of tetrasporogenesis documented in this study further challenge this dichotomy. Previous ultrastructural studies noted distinct perinuclear patterns in tetrasporangia of the coralline red algal genera Corallina. Jania. and Haliptilon (Peel et al 1973, Duckett and Peel 1978, Vesk and Borowitzka 1984) . Each investigation documented various stages of a single pattern of perinuclear ER (PER) with an associated electron-dense material (EDM) . This pattern is believed to be unique to the order Corallinales. The present study was conducted with two primary objectives. First, a detailed ultrastructural account of tetrasporogenesis in Bossiella orbigniana was completed. This work not only documented a previously undescribed PER/EDM pattern in a coralline alga, but also established the developmental framework for the second aspect of the study. Three non-geniculate and seven geniculate genera were surveyed to examine the extent of PER/EDM associations in coralline algae. A cursory phylogenetic analysis suggests that the classification of coralline red algae, with an emphasis on the presence or absence of genicula as a primary defining feature, may not be correct. ix PHYLOGENETIC IMPLICATIONS OF TETRASPORANGIAL ULTRASTRUCTURE IN CORALLINE RED ALGAE WITH REFERENCE TO BOSSIELLA ORBIGNIANA (CORALLINALES, RHODOPHYTA) INTRODUCTION The algal phylum Rhodophyta consists of a single class of organisms which range in structural complexity from unicells through psuedoparenchymatous upright thalli (Gabrielson et al 1991). The Rhodophyta are distinguished from other phyla of photosynthetic eukaryotes by the presence of chloroplasts with single, unstacked thylakoids, phycobilin pigments attached to thylakoids as phycobilisomes, floridean starch, and by a lack of flagellated structures at any life history stage (Gabrielson et al 1985; Gabrielson and Garbary 1986, 1987; Gabrielson et al 1991). Traditionally, taxonomists recognized two classes of red algae. The Bangiophyceae, considered the most primitive of the red algae, have been shown to lack shared, derived characteristics (synapormorphies) (Gabrielson et al 1985, Garbary and Gabrielson 1990) . The Florideophyceae, which consisted of the more morphologically advanced red algae, were, in contrast, united by at least two synapormorphic reproductive features (Gabrielson et al 1991) . Although, arguably, neither represents a valid taxonomic epithet, the terms "bangiophyte" and "florideophyte" continue to pervade systematic discussions of "primitive" and "advanced" red algal forms, respectively. Taxonomic schemes elucidating ordinal relationships 2 3 within the Rhodophyta have been proposed, but none has been unanimously accepted (Garbary and Gabrielson 1990, Gabrielson et al 1991) . The first ordinal classification schemes were principally derived from light microscopic studies on pre- and post- fertilization changes associated with female reproductive anatomy. Ongoing taxonomic revisions have stemmed from a new suite of traits revealed largely at the ultrastructural level. New knowledge of variations in the mitotic process, distinct organelle associations, and the fine structure of pit connections (unique regions of cytoplasmic continuity between cells) prompted a reevaluation of existing ordinal classification (Gabrielson and Garbary 1986). While molecular biology will undoubtedly generate further reevaluations of red algal systematics, morphological details of reproductive anatomy will likely continue to yield important classification information. Sporangia and spores can be considered evolutionarily conserved within the phylum Rhodophyta. Spores of various types are found in every rhodophycean order (Guiry 1990). Important features which serve to distinguish sporangia/spores include the number of nuclei in each spore, the number and arrangement of spores in a given sporangium, the position of a sporangium on the thallus, the presence or absence
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