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By H.D.V. PRENDERGAST a Thesis Submitted for the Degree of Doctor of Philosophy of the Australian National University. January 1

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By H.D.V. PRENDERGAST a Thesis Submitted for the Degree of Doctor of Philosophy of the Australian National University. January 1 STRUCTURAL, BIOCHEMICAL AND GEOGRAPHICAL RELATIONSHIPS IN AUSTRALIAN c4 GRASSES (POACEAE) • by H.D.V. PRENDERGAST A thesis submitted for the degree of Doctor of Philosophy of the Australian National University. January 1987. Canberra, Australia. i STATEMENT This thesis describes my own work which included collaboration with Dr N .. E. Stone (Taxonomy Unit, R .. S .. B.S .. ), whose expertise in enzyme assays enabled me to obtain comparative information on enzyme activities reported in Chapters 3, 5 and 7; and with Mr M.. Lazarides (Australian National Herbarium, c .. s .. r .. R .. O .. ), whose as yet unpublished taxonomic views on Eragrostis form the basis of some of the discussion in Chapter 3. ii This thesis describes the results of research work carried out in the Taxonomy Unit, Research School of Biological Sciences, The Australian National University during the tenure of an A.N.U. Postgraduate Scholarship. iii ACKNOWLEDGEMENTS My time in the Taxonomy Unit has been a happy one: I could not have asked for better supervision for my project or for a more congenial atmosphere in which to work. To Dr. Paul Hattersley, for his help, advice, encouragement and friendship, I owe a lot more than can be said in just a few words: but, Paul, thanks very much! To Mr. Les Watson I owe as much for his own support and guidance, and for many discussions on things often psittacaceous as well as graminaceous! Dr. Nancy Stone was a kind teacher in many days of enzyme assays and Chris Frylink a great help and friend both in and out of the lab •• Further thanks go to Mike Lazarides (Australian National Herbarium, c.s.I.R.O.) for identifying many grass specimens and for unpublished data on infrageneric groups in Eragrostis; Dr. John Busby (Bureau of Flora and Fauna, Canberra) for help and encouragement in the use of the Bioclima te Prediction Sy stem; Drs. David Coates and David Shaw (R.S.B.S.) for advice on cytological techniques; Drs. J.N. Burnell and M.D. Hatch (Division of Plant Industry, C.S.I.R.o., Csnberra) for discussions on enzyme assays; H.A. Nix (Division of Water and Land Resources, C.S.I.R.O., Csnberra) for discussions and permission to reproduce in part a published figure; Ross Cunningham (Statistics, The Faculties) for statistical advice; Jo Pask (Taxonomy Unit) for help with electron microscopy; Vindhya Amarasinghe (Taxonomy Unit) for information on microhair types in Eragrostis; the staff of the Electron Microscopy Unit and of the Plant Culture, Photography and Illustration Sections (R.S.B.S.); Elizabeth Robertson and Gillian Hines (Taxonomy Unit) for a lot of demanding typing; and Barbara Piper for putting it all together. I am grateful for the award of an A.N.U. Postgraduate Scholarship and thanks again to Paul, Les, Nancy and Chris. iv ABSTRACT I have studied aspects of the biology of Australian grasses (Poaceae) in relation to photosynthetic pathway. In a cytological investigation of interspecific relationships in the photosynthetically variable tribe Neurachneae (subfamily Panicoideae), the chromosomes of all species (C 3, c 3-c4 , c 4 l were found to be small (x= 2 µm) and either metacentric or submetacentric. The base number (x= 9) is typical for panicoid grasses; tetraploidy is the most common of the three ploidy levels (2x, 4x, 6x). Using the Bioclimate Prediction System, climatic profiles were compiled for each species anc: actual lnd predicted geographical distributions were mapped. In conjunction Jith selective biochemical sampling, a survey of c. 370 c 4 species was then undertaken to document them for leaf blade structural ueed as predictors of the three C 4 acid decarboxylat~on types Jf the c 4 pathway. In the largest Australian c 4 grass genus, Eragro.9tis (Chloridoideae), some species have features previously associated with the PEP carboxykinase type (PCK), but their main decarbo;:ylation enzyme is NAD-malic enzyme (NAD-ME) as in species with typical ('classical') NAD-ME anatomy. An intermediate structure is also described. Other NAD-ME species with broadly 'PCK-like' anatomy were found in Enneapogon, Triodia, Triraphis (Chloridoideae) and Paniewn (Panicoideaej. ALLoteropsis semialata (Panicoideae) is the first recorded PCK species with NADP-malic enzyme-like (NADP-ME) anatomy, and Eriaehne and Pheidoehloa (Arundinoideae) contain the first known NADP-ME species with anatomy like that of 'classical' NAD-ME or PCK species. A schematic summary of all currently known structural/biochemical associations in grasses is presented, and possible physiological implications with regard to the maintenance of a high [C0 2 J in PCR v (Photosynthetic Carbon Reduction, or Kranz) tissue are discussed. Chlorophyll a:b ratios from all biochemical experiments were statistically analysed. Means (and standard errors of the mean) for each c4 type are: NADP-ME, 4.45 (±0.04); NAD-ME, 4.01 (±0.03); PCK, 3.45 (±0.02). The differences between the means are statistically significant, even in cornpari sons across major taxonomic and/or anatomical groups. Cynoahloris m:iaivorii and C. reynoldsensis (Chloridoideae) are unusual examples of spontaneous intergeneric hybrids between parental species of different c4 types and leaf blade structures. Both were found to be structurally and biochemically intermediate between the 'iAD­ ME parent Cynodon daatylon and the PCK Chloris parent( s). Controlled, recriprocal crossing experiments between Cynodon and Chloris couC.,i explore genetic relationships between c4 types. Es ti mates were made of the total number of native Australian r: 4 grass species of each c4 type: NADP-ME, 348 species; NAD-ME, ;95 species; PCK, 65 species. All three types are most numerous in the mega therm seasonal bioclima te of northern Q.leensland. NADP-ME species dominate, species number-wise, in 48 out of 73 State and Territory subdivisions, with NAD-ME species dominant in the remainder (and codominant in two). NAD-ME species are proportionally at their most numerous in the megatherm/mesotherm arid bioclimate. The extent of the mega therm seasonal (rainfall) bioclimate is paralleled by :.r:e di stri bu ti on of most PCK species, by Eragrostis species with centrifugal/peripheral PCR cell chloroplasts, and by a relatively high proportion of species of all c 4 types with a suberized lamella in their PCR cell walls. The physiological reasons for these correlations are unknown. Taxonomic, ecological and historical factors in relation to c 4 type distribution are discussed. vi PRESENTATION OF THESIS Chapters are presented in the order in which they were written during the course of my studentship. Chapter 1 is a discursive overview of the thesis which is meant to convey chronological and personal aspects of its development. Each chapter has been prepared in the format of a paper for a scientific journal, complete with its own introduction and discussion, the latter also incorporating ideas for future research. Chapters 2 and 3 have, in fact, already been published and Chapter 4 has been accepted for publication. Subsequent to original publication of Chapter 2, new data became available as a result of a field-trip and these are incorporated into the text, tables and figures of the version presented here. Chapters 3 and 4, however, remain virtually unchanged from their published or accepted versions. The size of many tables has meant that photoreduction (from original A3 page size) was necessary. Tables and figures (and appendices in Chapter 2) are pooled at the end of each chapter (in that order), and references for all chapters are pooled at the end of the thesis. The format of presentation follows that of the C.S.I.R.O. journals. CONTENTS PAGE CHAPTER 1 OVERVIEW CHAPTER 2 DISTRIBUTION AND CYTOLOGY OF AUSTRALIAN NEURACHNE AND ITS ALLIES (POACEAE), A GROUP CONTAINING , c3 c4 AND C3-C4 INTERMEDIATE SPECIES. Abstract 10 Introduction 1 1 Materials and Methods 12 Results 14 Discussion 18 CHAPTER 3 ACID DECARBJXYIATION TYPE IN (POACEAE): c4 ERAGROS'rIS PATTERNS OF VARIATION IN CIILOROPIAST POSITION, l!]LTRASTRUCTURE AND GEDGRAPHICAL DISTRIBUTION. Abstract 24 Introduction 25 Materials and Methods 28 Results and Discussion 31 Concluding Remarks 38 CHAPTER 4 AUSTRALIAN C4 GRASSES (POACEAE): LEAF BLADE ANATOMICAL FEATURES IN RELATION TO ACID DECAROOXYIATION TYPES. c4 Abstract 42 Introduction 43 Materials and Methods 45 Results 46 Discussion 49 CHAPTER 5 NEii STRUCTURAL/BIOCHEMICAL ASSOCIATIONS IN LEAF BLADES OF c4 GRASSES (POACEAE). Abstract 56 Introduction 57 Materials and Methods 58 Results 59 Discussion 63 CHAPTER 6 WHOLE LEAF BLADE CllLOROPHYLL A:B RATIOS IN C4 GRASSES (POACEAE). Abstract 72 Introduction 73 Materials and Methods 74 Results 76 Discussion 77 CHAPTER 7 LEAF BLADE STRUCTURE AND C4 ACID DECAROOXYIATION ENZYMES IN CYNOCHWRIS SPP. (POACEAE), INTERGENERIC HmRIDS BETWEEN PARENTS OF DIFFERENT c 4 TYPES. Abstract 81 Introduction 82 Materials and Methods 83 Results 85 Discussion 87 CHAPTER 8 GIDGRAPHICAL DIS'rRIBOTION OF C ACID DECAROOXYLATION 4 TYPES AND ASSOCIATED S'rRcx::TORAL VARIANTS IN AUS'rRALIAN GRASSES (POACEAE). Abstract 89 Introduction 90 Methods and Sources of Data 92 Results 95 Discussion 107 REFERENCES 11 3 CHAPTER 1 OVERVIEW 1 I initially set out to address taxonomic and ecological aspects of variation in photosynthetic pathways via a cytogeographical analysis of the photosynthetically variable, endemic tribe Neurachneae (Chapter 2). I had hoped that cytological indications of the detailed interrelationships between the very closely related c , c and c -c 3 4 3 4 intermediate species might emerge, but it soon became clear that there was no future in this approach. The Neurachneae may well provide important clues to the evolution of c 4 photosynthesis but this will probably have to be pursued at the molecular level. I did, however, contribute to the small body of information on karyotypes of Australian grasses and, more interestingly, also highlighted the geographical distributions of the species of Neurachneae which are unusual in relation to photosynthetic pathways (see also Chapter 8) as well as peculiar in a taxonomic context.
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