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Theoretical Approach for the Developmental Basis of the Robustness and Stochasticity in Floral Organ Numbers

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Theoretical Approach for the Developmental Basis of the Robustness and Stochasticity in Floral Organ Numbers Theoretical Approach for the Developmental Basis Title of the Robustness and Stochasticity in Floral Organ Numbers Author(s) 北沢, 美帆 Citation Issue Date Text Version ETD URL https://doi.org/10.18910/52294 DOI 10.18910/52294 rights Note Osaka University Knowledge Archive : OUKA https://ir.library.osaka-u.ac.jp/ Osaka University Theoretical Approach for the Developmental Basis of the Robustness and Stochasticity in Floral Organ Numbers （花器官数の頑健性とばらつきを生み出す発生基盤の理論的探究） Kitazawa, Miho S. Laboratory of Theoretical Biology, Department of Biological Sciences, Graduate School of Science, Osaka University 大阪大学大学院理学研究科 生物科学専攻 理論生物学研究室 北沢美帆 Contents 4 Statistical Model Selection for Variation Curves of Floral Organ Numbers 45 Abstract iii 4.1 Abstract . 45 4.2 Introduction . 45 Publication List iv 4.3 Method . 46 1 General Remarks 1 4.3.1 Plant materials . 46 4.3.2 Models and their biological bases . 46 2 Developmental Model of Floral Organ 4.3.3 Model fitting and selection . 52 Number 6 4.4 Results . 53 2.1 Abstract . 6 4.4.1 Selection of the best statistical 2.2 Introduction . 6 model of the perianth-lobe number 2.3 Background . 6 variation in Ranunculaceae . 53 2.3.1 History of phyllotaxis studies . 7 4.4.2 Selection of the best model for 2.3.2 Floral organ positioning and phyl- variation curves of other clades lotaxis models . 12 and organs . 55 2.4 Model . 13 4.4.3 The parameters of the homeosis 2.5 Results of numerical simulations . 15 model . 55 2.6 Analytical results . 23 4.5 Discussion . 59 2.7 Discussion . 28 4.5.1 Developmental bases of the home- 2.7.1 Relevance and difference to phyl- osis model . 59 lotaxis models . 28 4.5.2 Counter examples of the homeosis 2.7.2 Propriety of assuming two inhibi- model . 59 tions . 28 2.7.3 The initiation potential and the 4.6 Future problems . 60 temporal decay of initiation inhi- 4.6.1 Improvement of the models. 60 bition . 28 4.7 Partial conclusion . 60 2.7.4 The growth potential and its bio- logical source. 30 5 General Conclusion and Relevance Be- 2.8 Future plan . 30 tween Chapters 61 2.9 Partial conclusion . 31 Appendix 63 3 Variation Curves and Their Statisticval Quantities in Floral Populations of Astera- A The Morphology of Angiosperm Aerial cae and Ranunculaceae 32 Parts 63 3.1 Abstract . 32 A.1 Phylogeny of angiosperms . 63 3.2 Background . 32 A.2 Shoot, basic structure of aerial part of an- 3.2.1 Statistical quantities and biologi- giosperms, and the foliar theory . 63 cal process . 32 A.3 Phyllotaxis . 65 3.2.2 Floral organ number variations . 32 A.3.1 Classifying phyllotaxis . 65 3.3 Method . 34 A.4 Vegetative Shoots . 67 3.3.1 Five basic statistical quantities . 34 A.4.1 Basic leaf structure . 67 3.3.2 Plant samples . 34 A.4.2 Variations in leaf shape . 68 3.4 Results . 35 A.5 Inflorescence . 69 3.4.1 Floral organ number variation in Ranunculaceae flowers . 35 A.5.1 Classification of inflorescence . 69 3.4.2 Floral organ number variation in A.5.2 Criteria for systematic classification 70 other clades . 38 A.6 Flower . 70 3.4.3 Relationship between SD and mean 41 A.6.1 Components of flower: floral organs 71 3.5 Discussion on floral organ number varia- A.6.2 Positional relationship between tion and statistical quantities . 43 floral components . 72 3.6 Partial conclusion . 44 A.6.3 Symmetry . 73 i B Development of Lateral Organ 74 B.3.4 Adaxial-abaxial patterning . 80 B.1 Meristem . 74 B.4 Contribution of mechanical properties for B.1.1 Organization . 74 organ development . 81 B.1.2 Initiation . 75 B.1.3 Maintenance. 76 B.5 Floral development . 82 B.2 Lateral organ formation at the concentra- B.5.1 Bracts . 82 tion maximum of plant hormone auxin . 76 B.5.2 Initiation order of organ primordia 83 B.2.1 Auxin polar transport . 76 B.2.2 Auxin biosynthesis . 77 B.5.3 ABCE model and its evolutionary B.3 Downstream of the auxin signalling . 79 conservation . 83 B.3.1 Switch to determinate state . 79 B.5.4 Development of zygomorphic flowers 86 B.3.2 Cell division and organ swelling . 79 General Index . 99 B.3.3 Boundary establishment and post- meristematic modification of organ Gene Name Index . 100 position . 79 Taxonomic Index . 101 ii Abstract How do multicellular organisms determine the number of body parts precisely during their devel- opment? The number, such as the finger number of human, the body-segment number in insects, and the floral organ number in plants, might have been constrained during their evolution by the ecological adaptation or the requirement of the developmental process. The determining process of the number of body part is a fundamental question in morphogenesis of organisms asking the relationship between evolution and development. I focused on the floral organ number in flowering plants (angiosperms), because of their fas- cinating features for studying the number-determination process. First, flower is a reproductive organ that regulates speciation by the reproductive isolation in evolutionary process. Second, the floral organ number is constrained to numbers specific to the phylogenetic clades. The floral organ number in eudicots, the most diverged clade in angiosperms, is four or five, whereas it is three in monocots and magnoliids, the rest clades. Thus the change of floral organ number may have led to the branching of eudicots, or the change of developmental process associated with the branch- ing may have changed the floral organ number. Either way, the floral organ number should have clue to elucidate how the developmental process affect the evolution, or is affected by the evolu- tion. Third, the floral organ number shows both robustness and stochasticity. Besides the specific modal number of floral organ is conserved within the clade, it varies even within an individual in some species. Therefore we can access this question from two sides, namely, the robustness and stochasticity, by employing floral organ number as a target. I employed the mathematical modelling approach to examine the robustness of floral organ number, focusing on the arrangement of floral organs. I consulted models of phyllotaxis, the arrangement of leaves around a stem, because of the similarity of developmental process between phyllotaxis and the floral organ arrangement. Integrating the phyllotaxis models and the floral development observed in eudicots, I proposed a mathematical model, and found that the four and five are robust to parameter change compared to other numbers. This result suggests that the dominance of four and five in eudicots comes from the properties of floral development. With respect to the stochasticity, I performed field observations for variations of floral organ numbers in wild populations. I calculated the statistical quantities for the data collected by myself and prior researchers, and found that there are four types of variations (symmetric, positively skewed, negatively skewed, and multi-modal variations), and there are three types in the relation- ship between the average number (mean) and degree of variation (standard deviation) among the populations. The latter implies that there are at least two sources of the stochasticity in floral organ numbers in the developmental process. I applied four models based on plausible develop- mental process to the variations and evaluated the best-fit model by statistical model selection. I found that the model selected as the best is different depending on organ-type and genera, and that a model I newly proposed based on the fate-determination process of floral organ primordia is selected in the highest frequency for the organ number variations. iii Publication List 1. Kitazawa, Miho S. and Fujimoto, Koichi. (2014) A Developmental basis for stochas- ticity in floral organ numbers. Frontiers in Plant Evolution and Development, 5:545. 2. Kitazawa, Miho S. and Fujimoto, Koichi. A dynamical phyllotaxis model to deter- mine floral organ number. accepted to PLOS Computational Biology. I am preparing a submission of the contents in Sec. 3 as follows: Kitazawa, Miho S. and Fujimoto, Koichi. The developmental robustness of lateral organ numbers and the species diversity | an integrated approach of statistical analysis and mathematical modelling. iv Angiospermmae Eudicots Core eudicots ), and the largest Asterids Rosids Monocots monocots Magnolids %UXQLDOHV ঈঝॽ॔৯ $SLDOHV ७জ৯ 3DUDFU\SKLDOHV ঃছॡজইॕ॔৯ 'LSVDFDOHV ঐॶ঒३९क़৯ $VWHUDOHV य़ॡ৯ (VFDOORQLDOHV ग़५ढ़টॽ॔৯ $TXLIROLDOHV ঔॳঀय़৯ %RUDJLQDFHDH ঒ছ१य़ఐ 6RODQDOHV ॼ५৯ /DPLDOHV ३९৯ *HQWLDQDOHV জথॻक़৯ *DUU\DOHV फ़জ॔৯ (ULFDOHV ॶॶ४৯ &RPDOHV ঑६य़৯ &DU\RSK\OODOHV ॼॹ३॥৯ 6DQWDODOHV অকॡॲথ৯ %HUEHULGRSVLGDOHV ঋঝঋজॻউ३५৯ 'LOOHQLDFHDH অডঔॻय़৯ 6D[LIUDJDOHV ঘय़ঀ३ॱ৯ 9LWDOHV ঈॻक़৯ *HUDQLDOHV ইक़ট९क़৯ 0\UWDOHV ইॺঔঔ৯ &URVVRVRPDWDOHV ॡটॵ९ঐ৯ 3LFUDPQLDOHV আॡছ঒ॽ॔৯ 6DSLQGDOHV ঒ॡট४৯ +XHUWHDOHV ইग़ঝॸ॔৯ %UDVVLFDOHV ॔ঈছॼ৯ 0DOYDOHV ॔ड़ॖ৯ =\JRSK\OODOHV ঁঐঅ३৯ 0DOSLJKLDOHV य़থॺছঀड़৯ 2[DOLGDOHV ढ़ॱং঑৯ &HODVWUDOHV ॽ३य़ॠ৯ )DEDOHV ঐও৯ 5RVDOHV ংছ৯ )DJDOHV ঈॼ৯ &XFXUELWDOHV क़জ৯ *XQQQHUDOHV ॢথॿছ৯ %X[DOHV ॶ।৯ 3URWHDOHV খঐঔफ़३৯ 6DELDFHDH ॔ডঈय़৯ 5DQXQFXODOHV य़থএक़।৯ &HUDWRSK\OODOHV ঐॶঔ৯ $FRUDOHV ३ঙक़ঈ৯ $OLVPDWDOHV ड़ঔॲढ़৯ 3HWULVDYLDOHV १ॡছॖ९क़৯ 'LRVFRUHDOHV খঐঀॖঔ৯ 3DQGDQDOHV ॱ॥ঀय़৯ /LOLDOHV ঘজ৯ $VSDUDJDOHV य़४ढ़ॡ३৯ 'DV\SRJRQDFHDH ॲ३এ०ॼఐ $UHFDOHV খ३৯ 3RDOHV ॖॿ৯ =LQJLEHUDOHV ३ঙक़फ़৯ &RPPHOLQDOHV ॶঘॡ१৯ &KORUDQWKDOHV ७থজঙक़৯ /DXUDOHV ॡ५ঀय़৯ 0DJQROLDOHV ঔॡঞথ৯ &DQHOODOHV ढ़ॿছ৯ 3LSHUDOHV ॥३ঙक़৯ $XVWUREDLOH\DOHV ॔क़५ॺটংॖঞখ৯ 1\PSKDHDOHV ५ॖঞথ৯ $PERUHOODOHV ॔থ঎ঞছ৯ 7URFKRGHQGUDOHV খঐॢঝঐ৯ composed by carpel(s) usually occupies , a monophyletic group with rather uniform ), monocotyledons ( gynoecium Basal eudicots core eudicots . The basal dicots G 1 Angiosperms, or so-called flowering plants, are largely divided ), which are the male organs to produce pollen, compose the androecium A The phylogenetic tree of angiosperms [15]. ( represented by Ranunculales, which is a paraphyly branched early in the eudicot stamens ). Eudicots is subdivided into Figure 1.1: eudicots basal eudicots , which is denoted by a single character (Fig.
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