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Regulation of chloroplast development during the greening process Yan Ji Umeå Plant Science Centre Department of Plant Physiology Umeå, Sweden, 2020 This work is protected by the Swedish Copyright Legislation (Act 1960:729) Dissertation for PhD ISBN: 978-91-7855-416-4 Electronic version available at: http://umu.diva-portal.org/ Printed by: Cityprint i Norr AB Umeå, Sweden, 2020 Everything you go through, grows you. -Robert Tew Table of Contents ABSTRACT .................................................................................................................. III LIST OF PAPERS .......................................................................................................... IV INTRODUCTION .......................................................................................................... 1 PHOTOSYNTHESIS AND THE CHLOROPLASTS ............................................................................ 1 THE EVOLUTION AND DEVELOPMENT OF CHLOROPLASTS ........................................................... 2 The origin of chloroplasts......................................................................................... 2 Chloroplast development in higher plants ............................................................... 3 LIGHT SIGNALLING PATHWAYS CONTROLLING CHLOROPLAST DEVELOPMENT .................................. 6 Repressors of chloroplast development in darkness ................................................ 6 Photoreceptors transmit light information to molecular signalling pathways that control chloroplast development ............................................................................. 8 Regulatory nuclear components involved in the regulation of chloroplast development .......................................................................................................... 11 THE IMPACT OF LIGHT SIGNALLING ON PLASTID TRANSCRIPTION ................................................ 15 Transcription machineries of plant chloroplasts .................................................... 15 The specific functions of the different plastid sigma factors ................................. 17 The roles of PAPs during chloroplast biogenesis .................................................... 17 AIMS ......................................................................................................................... 22 RESULTS AND DISCUSSION ....................................................................................... 23 A POWERFUL NEW EXPERIMENTAL SYSTEM TO STUDY CHLOROPLAST DEVELOPMENT ..................... 23 THE ROLE OF CRYPTOCHROME- AND PHYTOCHROME-MEDIATED LIGHT SIGNALLING PATHWAYS DURING CHLOROPLAST DEVELOPMENT ............................................................................................ 24 Role of cryptochrome light signalling pathways in chloroplast development ....... 24 Misregulation of bZIPs interfere with cotyledon development........................................ 24 bZIP16, bZIP68 and GBF1 regulate nuclear gene expression in response to light ............ 26 Involvement of CRYs on bZIPs regulation ......................................................................... 28 bZIP16 could alter the DNA-binding affinity via Cys330 and act as a repressor in de- etiolation .......................................................................................................................... 30 Role of phytochrome light signalling pathways in the expression of PEP components mediating plastid transcription ......................................................... 31 Modelling of PHYB-PIF3 response .................................................................................... 31 SIGs and PAPs follow the modelled PHYB/PIF3 regulated expression profile .................. 32 The role of PHYB-PIF3 in regulation of SIGs and PAPs required for plastid transcription 32 A COMPLEX INTERPLAY BETWEEN NEP AND PEP CONTROL CHLOROPLAST BIOGENESIS .................. 33 Expression profiles of plastid-encoded genes during the greening process ........... 34 i SIGs and PAP5 present in the nucleoids of dark grown cells .................................. 34 Presence of fully assembled PEP complex in proplastids and etioplasts ................ 35 Misregulation of PhAPGs in PEP-impaired mutants during early light response ... 36 CONCLUDING REMARKS AND FUTURE PERSPECTIVES .............................................. 41 ACKNOWLEDGEMENT ............................................................................................... 44 REFERENCES ............................................................................................................. 46 ii Abstract Upon light exposure, the expression of one-third of the nuclear-encoded genes is changing, including genes encoding many chloroplast-targeted proteins responsible for the initiation of plastid transcription and the establishment of photosynthesis. The control of the nuclear-encoded genes involved in the development of chloroplast is referred to as anterograde signalling. In my thesis work I have focused on both cryptochrome and phytochrome signalling pathways regulating the transcription of photosynthesis-related genes during chloroplast development. The results in the thesis demonstrate that several light-responsive nuclear transcription factors play a direct role in chloroplast development, and reveal the regulatory mechanism underlying the initiation of plastid photosynthetic gene expression. In this thesis, bZIP16 was found as a CRY1 interacting factor. Together with bZIP68 and GBF1, they regulate the expression of LHCBs and SIG5 through a blue light signalling pathway, promoting cotyledon opening and chloroplast development during de-etiolation. These findings provide novel insights into the role of bZIP transcription factors during chloroplast development with the involvement of the cryptochrome signalling pathway. To further investigate how the plastid photosynthetic gene expression is initiated, I focused on the role of two plastid RNA polymerases, nuclear- encoded plastid RNA polymerase (NEP) and plastid-encoded plastid RNA polymerase (PEP). By combining the PIF3-binding motif analysis, mathematic modelling and photoreceptor mutant analysis, we demonstrated a PHYB-PIF3 mediated regulation of the initial expression of the nuclear-encoded PEP components, SIGs and PAPs with the G-box/PBE-box as potential PIF3 binding- site. I have also demonstrated the presence of a fully assembled PEP complex in both proplastids and etioplasts using 2D BN/SDS-PAGE and its importance for the basal level of psaA and psbA transcription in darkness and during the early light response. iii List of papers I. Louise Norén Lindbäck, Yan Ji and Åsa Strand. The role of bZIP16, bZIP68 and GBF1 in regulation of nuclear photosynthetic genes. Manuscript (2020) II. Carole Dubreuil, Yan Ji, Åsa Strand and Andreas Grölund. A quantitative model of the phytochrome-PIF light signalling initiating chloroplast development. Scientific Reports 7, 13884 (2017). Paper II is licensed under the Creative Commons Attribution 4.0 International license. III. Yan Ji, Nóra Lehotai, Yanjun Zan, Carole Dubreuil, Manuel Guinea Díaz and Åsa Strand. A fully assembled PEP complex detected in etioplasts and proplastids in Arabidopsis. Physiologia Plantarum, DOI:10.1111/ppl.13256 (2020) Paper II and III are reprinted with kind permission of the publishers. The papers will be referred to by their roman numbers in the following text. iv Introduction Photosynthesis and the chloroplasts Photosynthesis, the process which plant or algae captures light and transfers light energy into chemical energy, is one of the most important energy sources to sustain life on earth. In plants and algae, photosynthesis physically occurs in an organelle called chloroplast that is only a few microns in size. By providing the majority of carbon source and oxygen, chloroplast is vital for many biological functions in plant vitality, seed set, growth and yield, and has a profound impact on our atmosphere and climate. The majority of chloroplasts are found in plant leaves, with a few occasions in the plant stems, where light absorption is possible but expected to be much less efficient. The chloroplast is characterized by its green colour as a result of highly accumulated chlorophyll and its own circular DNA. Many components essential for photosynthesis are encoded by its own circular DNA within the chloroplast. Chloroplasts, therefore, cannot be generated by plant cell during meiosis and mitosis but through the same method used by bacteria to propagate, binary fission (Osteryoung 2003; Waters and Langdale 2009). The chloroplast is surrounded by two phospholipid layers, the outer and inner membranes, together called chloroplast envelope. Besides the envelope that physically separate the chloroplast from the rest of the plant cell, extensively folded internal membranes interlaced with protein complexes exist. These are named as thylakoids, hosting light reactions of photosynthesis and surrounded by aqueous inner space known as thylakoid lumen. The stacks of thylakoids, named as grana, are connected by stromal lamellae. The space between the inner membrane and the thylakoid membrane system is filled with stroma, containing starch granules, enzymes and copies of circular DNA referred to as nucleoid (Fig. 1) (Sakamoto et al. 2008). 1 Figure 1. Labelled illustration (A) and electron microscopy image (B) of chloroplast structure. Scale bar = 0.5 µm. The evolution and development of
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