A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division

Abstract

Recently, the FtsZ protein, which is known as a key component in bacterial cell division, was reported to be involved in mitochondrial division in algae. In yeast and animals, however, mitochondrial fission depends on the dynamin-like proteins Dnm1p and Drp1, respectively, whereas in green plants, no potential mitochondrial division genes have been identified. BLAST searches of the nuclear and mitochondrial genome sequences of Arabidopsis thaliana did not find any obvious homologue of the ␣-proteobacterial-type ftsZ genes. To determine whether mitochondrial division of higher plants depends on a dynamin-like protein, we cloned a cDNA for ADL2b, an Arabidopsis homologue of Dnm1p, and tested its subcellular localization and its dominant-negative effect on mitochondrial division. The fusion protein of green fluorescent protein and ADL2b was observed as punctate structures localized at the tips and at the constriction sites of mitochondria in live plant cells. Cells expressing dominant-negative mutant ADL2b proteins (K56A and T77F) showed a significant fusion, aggregation, and͞or tubulation of mitochondria. We propose that mitochondrial division in higher plants is conducted by dynamin-like proteins similar to ADL2b in Arabidopsis. The evolutional points of loss of mitochondrial FtsZ and the functional acquisition of dynamin-like proteins in mitochondrial division are discussed.

FRIENDLY Regulates Mitochondrial Distribution, Fusion, and Quality Control in Arabidopsis

“…However, applying the same argument to Arabidopsis leads to the opposite conclusion. Arabidopsis mutants of proteins involved in mitochondrial division, such as the dynamin-like proteins Dynamin Related Protein 3A (DRP3A; Logan et al, 2004) and DRP3B (Arimura and Tsutsumi, 2002), the FISSION1 ortholog BIGYIN1 (Scott et al, 2006), or the plant-specific protein NETWORK MITOCHONDRIA1 Arimura et al, 2008), contain greatly enlarged, elongated, or reticular mitochondria, completely different from the clustered mitochondrial phenotype of friendly mutants. Notwithstanding the lack of evidence for a membranous connection between mitochondria in a cluster, the fact that clusters can move through the cytosol as units demonstrates that individual mitochondria in a cluster are physically associated, as suggested by our observation of electron-dense patches between mitochondria visualized by TEM.…”

“…A predominance of fusion over fission, caused by genetic deletion of components of the fission apparatus, leads to a more reticular network chondriome, while genetic deletion of components of the fusion apparatus in yeast and animal cells leads to a fragmentation of the chondriome (Shaw and Nunnari, 2002;Karbowski and Youle, 2003;Okamoto and Shaw, 2005;Hoppins and Nunnari, 2009). It is clear that disruption of mitochondrial fission in plants leads to the production of long, reticular mitochondria (Arimura and Tsutsumi, 2002;Logan et al, 2003Logan et al, , 2004Scott et al, 2006). However, we know nothing of the plant fusion apparatus.…”

The Arabidopsis peroxisome division mutantpdd2is defective in theDYNAMIN-RELATED PROTEIN3A(DRP3A) gene

“…10 The function of PEX11 seems to be exclusive to peroxisomes, whereas DRP3 and FIS1 are shared by the division machineries of both peroxisomes and mitochondria in Arabidopsis. 8,9,[11][12][13][14][15][16] FIS1 proteins are believed to tether DRP proteins to the peroxisomal membrane, 17,18 but direct evidence has not been obtained from plants. DRP3A and DRP3B share 77% sequence identity at the protein level and are functionally redundant in regulating mitochondrial division; however, DRP3A's role on the peroxisome seems stronger and cannot be substituted by DRP3B in peroxisome division.…”

The Mitochondrial Cycle of Arabidopsis Shoot Apical Meristem and Leaf Primordium Meristematic Cells Is Defined by a Perinuclear Tentaculate/Cage-Like Mitochondrion

“…Similarly, higher plant mitochondria have been typically portrayed as round to sausage-like organelles (Olyslaegers and Verbelen, 1998;Logan and Leaver, 2000;Nebenfü hr et al, 2000;Arimura and Tsutsumi, 2002;Van Gestel and Verbelen, 2002;Logan et al, 2003;Arimura et al, 2004;Logan, 2006a). Although some studies report on the presence of reticulate mitochondria in unperturbed eggs (Kuroiwa et al, 1996(Kuroiwa et al, , 2002 and vascular cell types (Gamalei and Pakhomova, 1981), most of the documented examples of reticular or disc-shaped mitochondria come from mitochondrial mutants (Arimura and Tsutsumi, 2002;Logan et al, 2003) or from cells subjected to experimental perturbations such as low oxygen pressure (Bereiter-Hahn, 1990;Van Gestel and Verbelen, 2002;Logan, 2006a), prolonged cell culturing (Rohr, 1978), or protoplasting (Sheahan et al, 2004(Sheahan et al, , 2005. It may be argued that the exposure of the root, stem, and shoot tissues to Suc (a cryoprotectant) in the growth and freezing medium prior to highpressure freezing might have produced the "reticulate" (tentaculate/cage-like) mitochondrial architecture observed in this study.…”