bims-plasge 2021-04-04 papers

Plant Cell. 2021 Jan 11. pii: koaa048. [Epub ahead of print]

GUN control in retrograde signaling: How GENOMES UNCOUPLED proteins adjust nuclear gene expression to plastid biogenesis.

Guo-Zhang Wu, Ralph Bock.

Communication between cellular compartments is vital for development and environmental adaptation. Signals emanating from organelles, so-called retrograde signals, coordinate nuclear gene expression with the developmental stage and/or the functional status of the organelle. Plastids (best known in their green photosynthesizing differentiated form, the chloroplasts) are the primary energy-producing compartment of plant cells, and the site for the biosynthesis of many metabolites, including fatty acids, amino acids, nucleotides, isoprenoids, tetrapyrroles, vitamins, and phytohormone precursors. Signals derived from plastids regulate the accumulation of a large set of nucleus-encoded proteins, many of which localize to plastids. A set of mutants defective in retrograde signaling (genomes uncoupled, or gun) was isolated over 25 years ago. While most GUN genes act in tetrapyrrole biosynthesis, resolving the molecular function of GUN1, the proposed integrator of multiple retrograde signals, has turned out to be particularly challenging. Based on its amino acid sequence, GUN1 was initially predicted to be a plastid-localized nucleic acid-binding protein. Only recently, mechanistic information on the function of GUN1 has been obtained, pointing to a role in plastid protein homeostasis. This review article summarizes our current understanding of GUN-related retrograde signaling and provides a critical appraisal of the various proposed roles for GUNs and their respective pathways.

DOI: https://doi.org/10.1093/plcell/koaa048

Plant Physiol. 2021 Jan 25. pii: kiaa106. [Epub ahead of print]

Knockdown of the plastid-encoded acetyl-CoA carboxylase gene uncovers functions in metabolism and development.

Rodrigo Caroca, Katharine A Howell, Irina Malinova, Asdrúbal Burgos, Nadine Tiller, Tommaso Pellizzer, Maria Grazia Annunziata, Claudia Hasse, Stephanie Ruf, Daniel Karcher, Ralph Bock.

De novo fatty acid biosynthesis in plants relies on a prokaryotic-type acetyl-CoA carboxylase (ACCase) that resides in the plastid compartment. The enzyme is composed of four subunits, one of which is encoded in the plastid genome, whereas the other three subunits are encoded by nuclear genes. The plastid gene (accD) encodes the β-carboxyltransferase subunit of ACCase and is essential for cell viability. To facilitate the functional analysis of accD, we pursued a transplastomic knockdown strategy in tobacco (Nicotiana tabacum). By introducing point mutations into the translational start codon of accD, we obtained stable transplastomic lines with altered ACCase activity. Replacement of the standard initiator codon AUG with UUG strongly reduced AccD expression, whereas replacement with GUG had no detectable effects. AccD knockdown mutants displayed reduced ACCase activity, which resulted in changes in the levels of many but not all species of cellular lipids. Limiting fatty acid availability caused a wide range of macroscopic, microscopic, and biochemical phenotypes, including impaired chloroplast division, reduced seed set, and altered storage metabolism. Finally, while the mutants displayed reduced growth under photoautotrophic conditions, they showed exaggerated growth under heterotrophic conditions, thus uncovering an unexpected antagonistic role of AccD activity in autotrophic and heterotrophic growth.

DOI: https://doi.org/10.1093/plphys/kiaa106

Plant Physiol. 2021 Jan 23. pii: kiaa109. [Epub ahead of print]

Biotin attachment domain-containing proteins mediate hydroxy fatty acid-dependent inhibition of acetyl CoA carboxylase.

Xiao-Hong Yu, Yuanheng Cai, Jantana Keereetaweep, Kenneth Wei, Jin Chai, Elen Deng, Hui Liu, John Shanklin.

Hundreds of naturally occurring specialized fatty acids (FAs) have potential as desirable chemical feedstocks if they could be produced at large scale by crop plants; however, transgenic expression of their biosynthetic genes has generally been accompanied by dramatic reductions in oil yield. For example, expression of castor (Ricinus communis) FA hydroxylase (FAH) in the Arabidopsis thaliana FA elongation mutant fae1 resulted in a 50% reduction of FA synthesis rate that was attributed to inhibition of acetyl-CoA carboxylase (ACCase) by an undefined mechanism. Here, we tested the hypothesis that the ricinoleic acid-dependent decrease in ACCase activity is mediated by biotin attachment domain-containing (BADC) proteins. BADCs are inactive homologs of biotin carboxy carrier protein that lack a biotin cofactor and can inhibit ACCase. Arabidopsis contains three BADC genes. To reduce expression levels of BADC1 and BADC3 in fae1/FAH plants, a homozygous badc1,3/fae1/FAH line was created. The rate of FA synthesis in badc1,3/fae1/FAH seeds doubled relative to fae1/FAH, restoring it to fae1 levels, increasing both native FA and HFA accumulation. Total FA per seed, seed oil content, and seed yield per plant all increased in badc1,3/fae1/FAH, to 5.8 µg, 37%, and 162 mg, respectively, relative to 4.9 µg, 33%, and 126 mg, respectively, for fae1/FAH. Transcript levels of FA synthesis-related genes, including those encoding ACCase subunits, did not significantly differ between badc1,3/fae1/FAH and fae1/FAH. These results demonstrate that BADC1 and BADC3 mediate ricinoleic acid-dependent inhibition of FA synthesis. We propose that BADC-mediated FAS inhibition as a general mechanism that limits FA accumulation in specialized FA-accumulating seeds.

DOI: https://doi.org/10.1093/plphys/kiaa109

RNA Biol. 2021 Mar 28.

RNA methylation in chloroplasts or mitochondria in plants.

Stefano Manduzio, Hunseung Kang.

Recent advances in our understanding of epitranscriptomic RNA methylation have expanded the complexity of gene expression regulation beyond epigenetic regulation involving DNA methylation and histone modifications. The installment, removal, and interpretation of methylation marks on RNAs are carried out by writers (methyltransferases), erasers (demethylases), and readers (RNA-binding proteins), respectively. Contrary to an emerging body of evidence demonstrating the importance of RNA methylation in the diverse fates of RNA molecules, including splicing, export, translation, and decay in the nucleus and cytoplasm, their roles in plant organelles remain largely unclear and are only now being discovered. In particular, extremely high levels of methylation marks in chloroplast and mitochondrial RNAs suggest that RNA methylation plays essential roles in organellar biogenesis and functions in plants that are crucial for plant development and responses to environmental stimuli. Thus, unveiling the cellular components involved in RNA methylation in cell organelles is essential to better understand plant biology.

Keywords: Chloroplast; Epitranscriptome; Mitochondria; RNA methylation; RNA modification

DOI: https://doi.org/10.1080/15476286.2021.1909321