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The thylakoid membrane protein NTA1 is an assembly factor of the cytochrome b6f complex essential for chloroplast development in Arabidopsis

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Plant Communications 2023年第1期4卷 287-303页

作者： Na Li Wing Shing Wong Lei Feng Chunming Wang King Shing Wong Nianhui Zhang Wei Yang Yueming Jiang Liwen Jiang Jun-Xian He School of Life Sciences and State Key Laboratory of Agrobiotechnology The Chinese University of Hong KongShatinNew TerritoriesHong Kong SARChina Key Laboratory of Bio-Resources and Eco-Environment of Ministry of Education College of Life SciencesSichuan UniversityChengduSichuanChina Guangdong Provincial Key Laboratory of Applied Botany&Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement Core Botanical GardensSouth China Botanical GardenChinese Academy of SciencesGuangzhouChina

The cytochrome b_(6f)(Cyt b_(6f))complex is a multisubunit protein complex in chloroplast thylakoid membranes required for photosynthetic electron transport.Here we report the isolation and characterization of the new tiny albino 1(nta1)mutant in Arabidopsis,which has severe defects in Cyt b_(6f) accumulation and chloroplast development.Gene cloning revealed that the nta1 phenotype was caused by disruption of a single nuclear gene,NTA1,which encodes an integral thylakoid membrane protein conserved across green algae and plants.Overexpression of NTA1 completely rescued the nta1 phenotype,and knockout of NTA1 in wild-type plants recapitulated the mutant phenotype.Loss of NTA1 function severely impaired the accumulation of multiprotein complexes related to photosynthesis in thylakoid membranes,particularly the components of Cyt b_(6f).NTA1 was shown to directly interact with four subunits(Cyt b6/PetB,PetD,PetG,and PetN)of Cyt b_(6f) through the DUF1279 domain and C-terminal sequence to mediate their assembly.Taken together,our results identify NTA1 as a new and key regulator of chloroplast development that plays essential roles in assembly of the Cyt b_(6f) complex by interacting with multiple Cyt b_(6f) subunits.

关键词： albino mutant chloroplast development cytochrome b6f complex assembly factor Arabidopsis thaliana

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An MCIA-like complex is required for mitochondrial complex Ⅰ assembly and seed development in maize

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Molecular Plant 2022年第9期15卷 1470-1487页

作者： Gang Wang Yongyan Wang Jiacheng Ni Rongrong Li Fengling Zhu Ruyin Wang Qiuzhen Tian Qingwen Shen Qinghua Yang Jihua Tang Monika W.Murcha Guifeng Wang National Key Laboratory of Wheat and Maize Crops Science CIMMYT--China Joint Center of Wheat and MaizeCenter for Crop Genome EngineeringCollege of AgronomyHenan Agricultural UniversityZhengzhou 450046China Shanghai Key Laboratory of Bio-Energy Crops School of Life SciencesShanghai UniversityShanghai 200444China School of Agriculture and Biology Shanghai Jiao Tong UniversityShanghai 200240China School of Molecular Sciences&The ARC Centre of Excellence in Plant Energy Biology The University of Western Australia35 Stirling HighwayCrawleyPerthWA 6009Australia The Shennong Laboratory ZhengzhouHenan 450002China

During adaptive radiation,mitochondria have co-evolved with their hosts,leading to gain or loss of subunits and assembly factors of respiratory complexes.Plant mitochondrial complex Ⅰ harbors40 nuclearand 9 mitochondrial-encoded subunits,and is formed by stepwise assembly during which different intermediates are integrated via various assembly factors.In mammals,the mitochondrial complex Ⅰ intermediate assembly(MCIA)complex is required for building the membrane arm module.However,plants have lost almost all of the MCIA complex components,giving rise to the hypothesis that plants follow an ancestral pathway to assemble the membrane arm subunits.Here,we characterize a maize crumpled seed mutant,crk1,and reveal by map-based cloning that CRK1 encodes an ortholog of human complex Ⅰ assembly factor 1,zNDUFAF1,the only evolutionarily conserved MCIA subunit in plants.zNDUFAF1 is localized in the mitochondria and accumulates in two intermediate complexes that contain complex Ⅰ membrane arm subunits.Disruption of zNDUFAF1 results in severe defects in complex Ⅰ assembly and activity,a cellular bioenergetic shift to aerobic glycolysis,and mitochondrial vacuolation.Moreover,we found that zNDUFAF1,the putative mitochondrial import inner membrane translocase ZmTIM17-1,and the isovaleryl-coenzyme A dehydrogenase ZmIVD1 interact each other,and could be co-precipitated from the mitochondria and co-migrate in the same assembly intermediates.Knockout of either ZmTIM17-1 or ZmIVD1 could lead to the significantly reduced complex Ⅰ stability and activity as well as defective seeds.These results suggest that zNDUFAF1,ZmTIM17-1 and ZmIVD1 probably form an MCIA-like complex that is essential for the biogenesis of mitochondrial complex Ⅰ and seed development in maize.Our findings also imply that plants and mammals recruit MCIA subunits independently for mitochondrial complex Ⅰ assembly,highlighting the importance of parallel evolution in mitochondria adaptation to their hosts.

关键词： assembly factor CIA30 evolution maize MCIA complex mitochondria seed development

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Structural insights into the functions of Raf1 and Bsd2 in hexadecameric Rubisco assembly

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Molecular Plant 2023年第12期16卷 1927-1936页

作者： Ran Wang Hui Song Wenjuan Zhang Ning Wang Shijia Zhang Ruiqi Shao Cuimin Liu State Key Laboratory of Plant Cell and Chromosome Engineering Institute of Genetics and Developmental BiologyThe Innovative Academy of Seed DesignChineseAcademyof SciencesBeijing100101China University of Chinese Academy of Sciences Bejing 100101China

Hexadecameric formI Rubisco,which consisting consists of eight large(RbcL)and eight small(RbcS)subunits,is the most abundant enzyme on earth.Extensive efforts to engineer an improved Rubisco to speed up its catalytic efficiency and ultimately increase agricultural productivity.However,difficulties with correct folding and assembly in foreign hosts or in vitro have hampered the genetic manipulation of hexadecameric Rubisco.In this study,we reconstituted Synechococcus sp.Pcc6301 Rubisco in vitro using the chaperonin system and assembly factors from cyanobacteria and Arabidopsis thaliana(At).Rubisco holoenzyme was produced in the presence of cyanobacterial Rubisco accumulation factor 1(Raf1)alone or both AtRaf1 and bundle-sheath defective-2(AtBsd2)from Arabidopsis.RbcL released from GroEL is assembly capable in the presence of ATP,and AtBsd2 functions downstream of AtRaf1.Cryo-EM structures of RbcL8-AtRaf18,RbcL8-AtRaf14-AtBsd2s,and RbcLs revealed that the interactions between RbcL and AtRaf1 are looser than those between prokaryotic RbcL and Raf1,with AtRaf1 tilting 7°farther away from RbcL.AtBsd2 stabilizes the flexible regions of RbcL,including the N and C termini,the 60s loop,and loop 6.Using these data,combined with previous findings,we propose the possible biogenesis pathways of prokaryotic and eukaryotic Rubisco.

关键词： Rubisco chaperone protein folding protein assembly assembly factor

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SNOWY COTYLEDON 2 Promotes Chloroplast Development and Has a Role in Leaf Variegation in Both Lotus japonicus and Arabidopsis thaliana

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Molecular Plant 2017年第5期10卷 721-734页

作者： Nicola Zagari Omar Sandoval-lbanez Niels Sandal Junyi Su Manuel Rodriguez-Concepcion Jens Stougaard Mathias Pribil Dario Leister Pablo Pulido Plant Molecular Biology Department of Biology I Ludwig-Maximilians-Universitat Munchen 82152 Planegg-Martinsried Germany Copenhagen Plant Science Center University of Copenhagen 1871 Frederiksberg C Denmark Research and Innovation Center Fondazione Edmund Mach via E. Mach 1 38010 San Michele all'Adige Italy Centre for Carbohydrate Recognition and Signalling Department of Molecular Biology and Genetics Aarhus University Gustav Wieds Vej 10 8000 Aarhus C Denmark Centre for Research in Agricultural Genomics (CRAG) CSIC-IRTA-UAB-UB Campus UAB Bellaterra 08193 Barcelona Spain

Plants contain various factors that transiently interact with subunits or intermediates of the thylakoid multiprotein complexes, promoting their stable association and integration. Hence, assembly factors are essential for chloroplast development and the transition from heterotrophic to phototrophic growth. Snowy cotyledon 2 （SCO2） is a DNAJ-like protein involved in thylakoid membrane biogenesis and interacts with the light-harvesting chlorophyll-binding protein LHCBI. In Arabidopsis thaliana, SCO2 function was previ- ously reported to be restricted to cotyledons. Here we show that disruption of SC02 in Lotus japonicus results not only in paler cotyledons but also in variegated true leaves. Furthermore, smaller and pale- green true leaves can also be observed in A. thaliana sco2 （atsco2） mutants under short-day conditions. In both species, SCO2 is required for proper accumulation of PSlI-LHCll complexes. In contrast to other variegated mutants, inhibition of chloroplastic translation strongly affects L. japonicus sco2 mutant devel- opment and fails to suppress their variegated phenotype. Moreover, inactivation of the suppressor of variegation AtClpR1 in the atsco2 background results in an additive double-mutant phenotype with variegated true leaves. Taken together, our results indicate that SCO2 plays a distinct role in PSll assembly or repair and constitutes a novel factor involved in leaf variegation.

关键词： SCO2 DNAJ-like photosynthesis assembly factor variegation chloroplast development

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Convergent evolution of factors for mitochondrial complex I assembly and safeguarding plant seed viability

Convergent evolution of factors for mitochondrial complex I ...

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第十九届中国作物学会学术年会

作者： Yongyan Wang Feiyu Ye Gang Wang Jiacheng Ni Jihua Tang Guifeng Wang

Eukaryotic mitochondria inherit from the Last Eukaryotic Common Ancestor(LECA). During adaptive radiation, mitochondria coevolve with their hosts, leading to gain and loss of subunits and assembly factors. Components of the Mitochondrial Complex I Intermediate assembly(MCIA) complex are indeed descended from various ancestors. Nevertheless, assembly factors and complex I assembly in plants are largely unknown. Here, we show that the only LECA-of-origin factor z NDUFAF1 has conserved function in complex I biogenesis. zNDUFAF1 disruption results in loss of complex I holoenzyme and activity, a striking bioenergetic shift to aerobic glycolysis, and seed abortion in maize. Homologs of Metazoa-of-origin factors, zTIMMDC1-1 and zACAD9, are found to mutually interact with z NDUFAF1 in mitochondria of maize endosperm cells. They comigrate and accumulate in several assembly intermediate complexes. Perturbations of z TIMMDC1-1 and z ACAD9-1 also lead to nonviable seeds. Thus, zNDUFAF1, zTIMMDC1-1 and zACAD9-1 are bona fide plant MCIA components essential for complex I assembly and seed development. Importantly, these assembly factors have different ancestral origins but with similar functions, suggesting convergent evolution of MCIA complex in animals and plants.

关键词： ACAD9 assembly factor CIA30 complex I evolution maize MCIA complex mitochondria seed development TIMMDC1-1

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