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Studies Into the Genetic Architecture of C3-C4 Characteristics in Moricandia

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Studies Into the Genetic Architecture of C3-C4 Characteristics in Moricandia Studies into the genetic architecture of C3-C4 characteristics in Moricandia Inaugural dissertation for the attainment of the title of doctor in the Faculty of Mathematics and Natural Sciences at the Heinrich Heine University Düsseldorf presented by Meng-Ying Lin from Taipei, Taiwan Düsseldorf, January 2020 From the institute of Plant Biochemistry at the Heinrich Heine University Düsseldorf Published by the permission of the Faculty of Mathematics and Natural Sciences at Heinrich Heine University Düsseldorf Supervisor: Prof. Dr. Andreas P.M. Weber Co-supervisor: Prof. Dr. Miltos Tsiantis Date of the oral examination: 05.05.2020 Declaration of the Doctoral Dissertation I herewith declare under oath that this dissertation was the result of my own work without any unauthorized help in compliance with the “Principles for the Safeguarding of Good Scientific Practice at Heinrich Heine University Düsseldorf”. This dissertation has never been submitted in this or similar format to any other institutions. I have not previously failed a doctoral examination procedure. Düsseldorf, 23.12.2019 Meng-Ying Lin Table of Contents I. Summary ............................................................................................................................... 1 II. Introduction ......................................................................................................................... 3 1. Motivation ....................................................................................................................................... 3 2. An overview of evolutionary trajectory from C3, C3-C4, toward C4 photosynthesis ................ 4 2.1 The photosynthetic pathway and problems resulting from photorespiration ............................ 4 2.2 The CO2 concentrating mechanism implemented in C3-C4 intermediate species ...................... 4 2.3 C4 plants evolve an efficient solution to repress photorespiration ............................................. 6 2.4 The evolutionary trajectory from C3 to C4 photosynthesis through C3-C4 intermediates .......... 8 3. Known genetic control of Kranz anatomy and chloroplast development ................................. 9 3.1 Regulation of Kranz anatomy development .............................................................................. 9 3.2 Genes related to chloroplast development, division, and movement ...................................... 11 4. Old stories and new expects of experimental hybrids in C3-C4/C4 gene discovery ................ 15 4.1 Efforts have been done in the past ........................................................................................... 15 4.2 A new experimental hybrid studying system in the Brassicaceae: Moricandia ...................... 15 4.3 Obstacles and new opportunities of the application of experimental hybrids ......................... 16 5. Strategies for genetic discovery of C3-C4 characteristics .......................................................... 17 5.1 Exploring regulatory divergences between different photosynthesis types ............................ 17 5.2 Comparative transcriptomics of closely related photosynthesis species ................................. 18 III. Aim of the Thesis ............................................................................................................. 21 IV. References ......................................................................................................................... 22 V. Manuscripts ....................................................................................................................... 33 1. Manuscript I: Interspecific Hybridization between Moricandia C3 and C3-C4 Species ........ 34 2. Manuscript II: Transcriptional Regulation Associated with the CO2 Concentrating Mechanism in Moricandia ............................................................................................................... 61 3. Manuscript III: Comparative Transcriptome Analysis during Leaf Development on Closely Related C3 and C3-C4 Moricandia Species .................................................................................... 115 VI. Acknowledgements ........................................................................................................ 161 I. Summary C3-C4 intermediate species are of great value to unravel molecular mechanisms of the early evolutionary steps of C4 photosynthesis, owing to the fact that they are predicted to be natural occurring intermediates on the convergent evolution from C3 to C4 photosynthesis. C3-C4 plants possess Kranz-like anatomy, bundle sheath cells with numerous organelles arranged centripetally around the veins, which serves as a requisite for the photorespiratory glycine shuttle. The P-subunit of the photorespiratory enzyme glycine decarboxylase is absent in C3- C4 mesophyll cells. In order to digest the toxic product 2-phosphogylcolate, the photorespiratory glycine is shuttled from mesophyll to bundle sheath cells, where the released CO2 can be efficiently recaptured by numerous, adjacent chloroplasts. Transcriptional regulation of spatial expression pattern of the P-protein of glycine decarboxylase between C3 and C3-C4 species is well known in Flaveria and Moricandia. However, the genetic architecture of C3-C4 characteristics remains largely elusive. In this thesis, I investigated cytogenetic characteristics of Moricandia C3 and C3-C4 species and the potential of interspecific hybridization between C3 and C3-C4 plant, serving as fundamental knowledge for further transcriptional regulation analysis and comparative transcriptomics. Different interspecific hybridizations between C3 and C3-C4 species in Moricandia were performed, where the hybridized pair of C3-C4 M. arvensis as maternal and C3 M. moricandioides as paternal species was the most prolific combination. To investigate C3-C4 intermediate specific gene expression, allele specific expression analysis was applied to the interspecific hybrids of M. arvensis and M. moricandioides. It demonstrated that cis- mechanisms play an important role in shaping C3 to C3-C4 photosynthesis type and the corresponding transcripts are enriched in major photosynthetic pathways and chloroplast relocation. Candidates with strong allele specific expression are of special interest for studying the genetic architecture regarding C3-C4 characteristic traits. Comparison of anatomical changes during leaf ontology between C3 and C3-C4 Moricandia species revealed the early establishment of Kranz-like anatomy in C3-C4 species. Through the comparative transcriptome and cluster analysis during leaf development of closely related C3 and C3-C4 Moricandia species, we found transcription factors as potential candidates for genetic control of C3-C4 characteristics, such as auxin response, sigma-like, and growth- related factor, and a cohort of genes regulating vein initiation, procambium formation, xylem 1 I. Summary formation, SCR/SHR pathway, and vein patterning associated with the early leaf development in C3-C4 M. arvensis. The early organelle accumulation in C3-C4 bundle sheath cells was more relevant to plastid division than formation and biosynthesis. 2 II. Introduction 1. Motivation The green revolution in the late 1960s resulted in a large increase of rice and wheat production through introduction of the dwarfing genes (Khush, 1999; Furbank et al., 2015; Nagai et al., 2018). The dwarfing genes are responsible for increasing yield by the reduction of lodging and for increasing of the harvest index in rice and wheat (Parry et al., 2011). The approach could also be implemented in Brassica crops (Muangprom et al., 2005). However, the increase of global production through improving harvest index is limited. The new generation of green revolution has focused on the increase of the biomass by improving the photosynthetic performance (Parry et al., 2011). C4 photosynthetic plant species outperform the ancestral C3 plants through considerable reduction of the energy-demanding photorespiration, which leads to a net loss of CO2 and decreases the efficiency of photosynthesis by 40% under ambient CO2 concentration and under conditions of water deficits and high temperatures (Gowik and Westhoff, 2011). Although the C4 photosynthetic pathway is found in only 3% of terrestrial plants, it accounts for around 25% of primary productivity (Still et al., 2003; Sage, 2004; Edwards et al., 2010). It has been predicted that the crop yield could be boosted by 50% with an increase of 10% the photosynthetic efficiency through transferring the C4 photosynthesis pathway into C3 crops (Langdale, 2011; Furbank et al., 2015). Many efforts have been done in producing C4 rice (von Caemmerer et al., 2012). However, the genetic control of C4 characters remains largely unknown, especially the molecular mechanisms regulating Kranz anatomy development. C3-C4 species are considered as naturally occurring intermediates on the evolutionary trajectory from C3 to C4 photosynthesis, possessing Kranz-like leaf anatomy and photorespiratory glycine shuttle, a CO2 concentrating mechanism. A recent model suggested that introduction of C3-C4 characters into C3 rice might be an advantageous alternative (Bellasio and Farquhar, 2019). Therefore, dissecting the genetic control of C3-C4 characters is not only prominent for understanding the early evolution of the C4 photosynthesis, but also for improving the breeding of highly efficient C3 crops through introducing C3-C4 characters. 3 II. Introduction 2. An overview of evolutionary
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