Mitochondrial Transcriptome Control and Intercompartment Cross-Talk During Plant Development
Abstract
1. Introduction
2. Materials and Methods
2.1. Preparation of Gene Constructs for In Vivo Expression
2.2. Nuclear Transformations
2.3. Seedling Growth and Trangene Induction
2.4. RNA Extraction, Northern Bloting and RT-qPCR Analyses
2.5. Isolation of Mitochondria and Import Assessment
2.6. Microarray Assays
2.7. Microarray Data Analyses
3. Results
3.1. Trans-Ribozyme-Mediated Modulation of Mitochondrial RNA Steady State Levels Depends on the Plant Developmental Stage
3.2. CMS RNA-Triggered Modulation of Mitochondrial RNA Steady State Levels Depends on the Plant Developmental Stage
3.3. Ribozyme-Mediated Knockdown of a Mitochondrial mRNA Triggers a Nuclear Transcriptome Response
4. Discussion
5. Conclusions
6. Patents
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Conditions and Developmental Stage | Day 1 | Day 2 | Day 3 | Day 4 |
---|---|---|---|---|
Light Early stage | ↓nad5a* | |||
↓atp4** | ||||
↑rps7* | ||||
↑AOX1d* | ↓AOX1d*** | ↓AOX1d*** | ||
Light Intermediate stage | ↑cob** | ↑rps7* | ||
↑nad5a** | ↓ccmFN2*** | ↑rpl2** | ||
↑nad5b** | ↑atp4* | ↑rpl5* | ||
↓ccmFN2** | ↑rpl2* | |||
↑rpl5* | ||||
↑AOX1d*** | ↑AOX1d*** | |||
Light Bolting stage | ↓nad2b** | ↓atp4* | ↑nad1b* | |
↑nad5a** | ↓atp9**** | ↓nad2b* | ||
↓nad5b** | ↓rps4** | ↓nad4** | ||
↓nad9** | ↓rps7**** | ↑nad5a*** | ||
↓cox1** ↓ccmB** | ↓rpl2**** | ↓nad5b* | ||
↓mttB* | ↓rpl5** | ↓nad6* | ||
↓rpl5* | ↓rrn18** | ↓nad9** | ||
↓cob*** | ||||
↓cox1* | ↓cox1**** | |||
↓cox2** | ↓atp9* | |||
↓cox3**** | ↓ccmFC*** | |||
↑atp9* | ↑mttB* | |||
↓ccmB*** | ↑rpl5** | |||
↓ccmFC* | ↓rrn26* | |||
↓ccmFN1*** | ||||
↓ccmFN2** | ||||
↓mttB** | ||||
↓rrn18*** | ||||
↓rrn26** | ||||
↓AOX1a* | ||||
↓AOX1d** | ↓AOX1d* | ↓AOX1d* | ||
Dark | ↑nad2b** | ↑nad4* | ↓nad1b*** | ↓ccmFC*** |
↓nad5a** | ↑nad5b* | ↓nad2b** | ↓matR* | |
↑nad5b**** | ↑cox1* | ↑nad5b** | ↓mttB* | |
↑nad9* | ↓ccmFN2** | ↓ccmFN2** | ↓rrn18**** | |
↓cox2* | ↓mttB** | ↑rrn26** | ||
↓matR* | ↓rrn26** | |||
↑rps7** | ||||
↓rpl5* | ||||
↓rrn26* | ||||
↑AOX1d** |
Modulation | Annotation / Function / Organellar Localization | Gene |
---|---|---|
Upregulated (opposite to nad9) | Basic helix-loop-helix (bHLH) DNA-binding superfamily protein; transcription factor; response to ethylene | AT1G05710 |
ABI3-interacting protein 3, AIP3, PFD4, PREFOLDIN 4; protein chaperone; ABI3 is an auxin-inducible transcription factor | AT1G08780 | |
ATMYB60, Myb domain protein 60, MYB60; transcription factor; response to abscisic acid, jasmonic acid, salicylic acid | AT1G08810 | |
Agamous-like 87, AGL87, MADS-box family protein; transcription factor | AT1G22590 | |
GL2, GLABRA 2, HD-ZIP IV family of homeobox-leucine zipper protein with lipid-binding START domain; transcription factor | AT1G79840 | |
DREB subfamily A-6 of ERF/AP2 transcription factor family; one AP2 domain; ethylene-activated | AT2G22200 | |
AP2/B3-like transcriptional factor family protein; transcription factor | AT2G33720 | |
FMA (FAMA), basic helix-loop-helix (bHLH) DNA-binding superfamily protein; transcription factor/ transcriptional activator | AT3G24140 | |
EDF3, ethylene response DNA-binding factor 3; transcription factor; AP2 domain; ethylene responding | AT3G25730 | |
IAA30, indole-3-acetic acid inducible protein 30; transcription factor; response to auxin | AT3G62100 | |
B-BOX domain protein 23, BBX23; transcription factor | AT4G10240 | |
PUCHI, ethylene response factor (ERF) subfamily B-1 of ERF/AP2 transcription factor family; one AP2 domain; ethylene response | AT5G18560 | |
ARGOS, Auxin-regulated gene involved in organ size; response to ethylene, auxin; membrane, cytoplasm, mitochondrion | AT3G59900 | |
EMB3103, Embryo-defective 3103, PDM2, Pigment-Defective Mutant2; pentatricopeptide repeat (PPR) superfamily protein; endonuclease; chloroplast/mitochondrion | AT1G10910 | |
RNH1C, RNase H family protein, RNase H domain-containing protein; chloroplast | AT1G24090 | |
RING-finger, DEAD-like helicase, PHD and SNF2 domain-containing protein | AT2G40770 | |
AT-SR34B, Serine/arginine-rich protein splicing factor 34B, SR34B | AT4G02430 | |
Mitochondrial nuclease 1, MNU1; putative endonuclease or glycosyl hydrolase; mitochondrial RNA 5'-end processing; chloroplast/mitochondrion | AT5G64710 | |
EMB2394, Embryo-defective 2394; structural constituent of chloroplast ribosome; response to cytokinin | AT1G05190 | |
rRNA, cytosolic small ribosomal subunit | AT2G01010 | |
5.8S rRNA, cytosolic large ribosomal subunit | AT2G01020 | |
40S ribosomal protein S23 (RPS23A), ribosomal protein S12/S23 family protein; cytosolic small ribosomal subunit | AT3G09680 | |
Ribosomal protein L15, RPL15; large subunit of the chloroplast ribosome; response to cytokinin | AT3G25920 | |
EMB3126, Embryo-defective 3126, plastid ribosomal protein L1, PRPL1; ribosomal protein L1p/L10e family; chloroplast large ribosomal subunit | AT3G63490 | |
60S ribosomal protein L31, RPL31B; cytosolic large ribosomal subunit | AT4G26230 | |
U3 ribonucleoprotein, Utp family protein; rRNA processing | AT5G08600 | |
MA3 domain-containing translation regulatory factor 1, MRF1; colocalizes with cytosolic large ribosomal subunit; isomerase activity | AT5G63190 | |
snoRNA | AT1G03743; AT1G19373; AT1G19376; AT1G75166; AT2G35387; AT3G27865; AT3G47342; AT3G47347; AT3G58193; AT3G58196; AT4G39366; AT5G44286 |
Modulation | Annotation/Function/Organellar Localization | Gene |
---|---|---|
Downregulated (as nad9) | MicroRNA414, mir414, short open reading frame 16, SORF16; miRNA; identified as a translated small open reading frame by ribosome profiling | AT1G67195 |
B-BOX domain protein 25, BBX25, Salt tolerance homologue, STH; transcription factor; zinc ion binding | AT2G31380 | |
ATIBH1, IBH1, ILI1 binding BHLH 1 ILI1 binding bHLH 1; transcription factor; brassinosteroid signaling; gibberellic acid signaling | AT2G43060 | |
Arabidopsis thaliana response regulator 2, ARR5, ATRR2, IBC6, induced by cytokinin 6, response regulator 5, RR5; transcription repressor; cytokinin signaling | AT3G48100 | |
Basic helix-loop-helix (bHLH) DNA-binding superfamily protein; transcription factor | AT4G01460 | |
KELP; homodimers or heterodimers with the kiwi protein; transcriptional co-activator | AT4G10920 | |
WRKY DNA-binding protein 24, ATWRKY24, WRKY24; WRKY transcription factor group II-c | AT5G41570 | |
BOA, Brother of lux ARRHYTHMO; transcription factor; circadian clock; mRNA cell-to-cell mobile | AT5G59570 | |
SAUR53, small auxin-upregulated RNA 53, SAUR-like auxin-responsive protein family; mitochondrion | AT1G19840 | |
SAUR65, small auxin-upregulated RNA 65, SAUR-like auxin-responsive protein family; membrane; mitochondrion | AT1G29460 | |
ATCLE19, CLAVATA3/ESR-related 19, CLE19, embryo surrounding region 19, ESR19; receptor binding; signal transduction; mitochondrion | AT3G24225 | |
VQ motif-containing protein 29, VQ29; response to hypoxia | AT4G37710 | |
RNA-binding (RRM/RBD/RNP motifs) family protein | AT1G33470 | |
ATRNS1, Ribonuclease 1, RNS1; endoribonuclease | AT2G02990 | |
Eukaryotic translation initiation factor 2 (eIF-2) family protein; cytosol | AT1G76820 | |
EMB3113, Embryo-defective 3113, ribosomal protein S5, RPS5, SCA1, SCABRA 1; structural component of the 70S chloroplast ribosome; mitochondrial small ribosomal subunit | AT2G33800 | |
U3 containing 90S pre-ribosomal complex subunit | AT2G43110 | |
ATRAB8D, ATRABE1B, RAB GTPase homolog E1B, RABE1B; translation elongation factor; membrane; chloroplast | AT4G20360 | |
snoRNA | AT2G35382; AT2G43137; AT2G43138; AT2G43139; AT2G43141; AT4G02550; AT4G02555; AT4G13245 |
Modulation | Annotation/Function/Organellar Localization | Gene |
---|---|---|
Upregulated (opposite to nad9) | Small nuclear RNA U6acat, mRNA splicing | AT5G40395 |
Downregulated (as nad9) | ANAC028, NAC domain-containing protein 28, NAC028; transcription factor | AT1G65910 |
Transcription elongation factor Spt5; KOW domain | AT2G34210 | |
MYR2, homeodomain-like superfamily protein; transcription factor | AT3G04030 | |
HVA22-like protein F, HVA22F; membrane protein; response to abscisic acid | AT2G42820 | |
ALY2 RNA-binding (RRM/RBD/RNP motifs) family protein; mRNA transport | AT5G02530 |
Modulation | Annotation/Function/Organellar Localization | Gene |
---|---|---|
Upregulated (opposite to nad9) | auxin-responsive family protein (SAUR72) | AT3G12830 |
auxin-responsive protein, putative (SAUR9) | AT4G36110 | |
auxin-responsive family protein (SAUR41) | AT1G16510 | |
auxin-responsive protein-related (SAUR77) | AT1G17345 | |
auxin-responsive family protein (SAUR53); mitochondrion | AT1G19840 | |
auxin-responsive family protein (SAUR71) | AT1G56150 | |
auxin-responsive family protein (SAUR52); mitochondrion | AT1G75590 | |
auxin-responsive protein-related (SAUR36); mitochondrion/nucleus (nucleus confirmed by GFP targeting experiments) | AT2G45210 | |
auxin-responsive family protein (SAUR59); mitochondrion | AT3G60690 | |
auxin-responsive protein, putative (SAUR25); mitochondrion | AT4G13790 | |
auxin-responsive family protein (SAUR1); chloroplast | AT4G34770 | |
auxin-responsive protein, putative (SAUR23) | AT5G18060 | |
MIF1 (MINI ZINC FINGER 1); transcription factor; response to abscisic acid, auxin, brassinosteroid, cytokinin, gibberellin; nucleus (cytosol reported from GFP data) | AT1G74660 | |
PLS (POLARIS), cytokinin and auxin responses; mitochondrion | AT4G39403 | |
Tetratricopeptide repeat (TPR)-like superfamily protein; mitochondrion | AT1G28690 | |
S-RBP11, SMALL RNA-BINDING PROTEIN 11; salt stress response; chloroplast | AT5G06210 | |
Downregulated (as nad9) | ARGAH2, Arginine amidohydrolase 2, response to jasmonate; chloroplast/mitochondrion (confirmed by MS data) | AT4G08870 |
Tetratricopeptide repeat (TPR)-like superfamily protein; chloroplast/mitochondrion (chloroplast confirmed by MS data) | AT2G37230 | |
pentatricopeptide (PPR) repeat-containing protein | AT3G62470 | |
pentatricopeptide (PPR) repeat-containing protein | AT4G01030 | |
EMB1417 (embryo-defective 1417), PPR protein; RNA binding; endonuclease activity | AT4G21190 | |
pentatricopeptide (PPR) repeat-containing protein | AT4G21880 | |
pentatricopeptide (PPR) repeat-containing protein | AT5G65560 | |
EMB1586, Embryo-defective 1586, increased size exclusion limit 1, ISE1; DEAD-box RNA helicase; chloroplast/mitochondrion (mitochondrion confirmed by GFP data) | AT1G12770 | |
AGS1, AHG2-1 suppressor 1, bacterial-type poly(A) polymerase; mRNA polyadenylation; chloroplast/mitochondrion | AT2G17580 | |
ATTRM2A, TRM2A, tRNA methyltransferase 2A, RNA methyltransferase family protein; cytoplasm | AT3G21300 | |
ATP-dependent RNA helicase | AT5G39840 | |
ARFB1A, ATARFB1A (ADP-ribosylation factor B1A); GTP binding; protein transport; Golgi apparatus | AT2G15310 |
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Niazi, A.K.; Delannoy, E.; Iqbal, R.K.; Mileshina, D.; Val, R.; Gabryelska, M.; Wyszko, E.; Soubigou-Taconnat, L.; Szymanski, M.; Barciszewski, J.; et al. Mitochondrial Transcriptome Control and Intercompartment Cross-Talk During Plant Development. Cells 2019, 8, 583. https://doi.org/10.3390/cells8060583
Niazi AK, Delannoy E, Iqbal RK, Mileshina D, Val R, Gabryelska M, Wyszko E, Soubigou-Taconnat L, Szymanski M, Barciszewski J, et al. Mitochondrial Transcriptome Control and Intercompartment Cross-Talk During Plant Development. Cells. 2019; 8(6):583. https://doi.org/10.3390/cells8060583
Chicago/Turabian StyleNiazi, Adnan Khan, Etienne Delannoy, Rana Khalid Iqbal, Daria Mileshina, Romain Val, Marta Gabryelska, Eliza Wyszko, Ludivine Soubigou-Taconnat, Maciej Szymanski, Jan Barciszewski, and et al. 2019. "Mitochondrial Transcriptome Control and Intercompartment Cross-Talk During Plant Development" Cells 8, no. 6: 583. https://doi.org/10.3390/cells8060583
APA StyleNiazi, A. K., Delannoy, E., Iqbal, R. K., Mileshina, D., Val, R., Gabryelska, M., Wyszko, E., Soubigou-Taconnat, L., Szymanski, M., Barciszewski, J., Weber-Lotfi, F., Gualberto, J. M., & Dietrich, A. (2019). Mitochondrial Transcriptome Control and Intercompartment Cross-Talk During Plant Development. Cells, 8(6), 583. https://doi.org/10.3390/cells8060583