Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes.

Mark P Simmons,Dale N Richardson,Anireddy SN Reddy

doi:10.1186/1471-2164-7-18

Abstract

BackgroundKinesins, a superfamily of molecular motors, use microtubules as tracks and transport diverse cellular cargoes. All kinesins contain a highly conserved ~350 amino acid motor domain. Previous analysis of the completed genome sequence of one flowering plant (Arabidopsis) has resulted in identification of 61 kinesins. The recent completion of genome sequencing of several photosynthetic and non-photosynthetic eukaryotes that belong to divergent lineages offers a unique opportunity to conduct a comprehensive comparative analysis of kinesins in plant and non-plant systems and infer their evolutionary relationships.ResultsWe used the kinesin motor domain to identify kinesins in the completed genome sequences of 19 species, including 13 newly sequenced genomes. Among the newly analyzed genomes, six represent photosynthetic eukaryotes. A total of 529 kinesins was used to perform comprehensive analysis of kinesins and to construct gene trees using the Bayesian and parsimony approaches. The previously recognized 14 families of kinesins are resolved as distinct lineages in our inferred gene tree. At least three of the 14 kinesin families are not represented in flowering plants. Chlamydomonas, a green alga that is part of the lineage that includes land plants, has at least nine of the 14 known kinesin families. Seven of ten families present in flowering plants are represented in Chlamydomonas, indicating that these families were retained in both the flowering-plant and green algae lineages.ConclusionThe increase in the number of kinesins in flowering plants is due to vast expansion of the Kinesin-14 and Kinesin-7 families. The Kinesin-14 family, which typically contains a C-terminal motor, has many plant kinesins that have the motor domain at the N terminus, in the middle, or the C terminus. Several domains in kinesins are present exclusively either in plant or animal lineages. Addition of novel domains to kinesins in lineage-specific groups contributed to the functional diversification of kinesins. Results from our gene-tree analyses indicate that there was tremendous lineage-specific duplication and diversification of kinesins in eukaryotes. Since the functions of only a few plant kinesins are reported in the literature, this comprehensive comparative analysis will be useful in designing functional studies with photosynthetic eukaryotes.

Highlights

Kinesins, a superfamily of molecular motors, use microtubules as tracks and transport diverse cellular cargoes
Flowering plants have the largest number of kinesins, three or four of the 14 kinesin families are not represented in flowering plants whereas three of them may not be present in any photosynthetic eukaryote
Among the 19 species analyzed, seven represent phylogenetically divergent photosynthetic eukaryotes that belong to monocots, dicots (Arabidopsis thaliana and Populus trichocarpa), a chlorophyte alga (Chlamydomonas reinhardtii), a red alga (Cyanidioschyzon merolae) and a diatom (Thalassiosira pseudonana)

Summary

Introduction

A superfamily of molecular motors, use microtubules as tracks and transport diverse cellular cargoes. Molecular motors that organize and remodel cytoskeleton and transport various cellular components (e.g, vesicles, organelles, chromosomes, RNA and protein complexes) play fundamental roles in all aspects of cell and developmental biology of eukaryotes [1,2]. Molecular motors that function on cytoskeletal networks belong to three groups: kinesins, dyneins and myosins These motors utilize energy derived from ATP hydrolysis and transport cargo unidirectionally on one of the filamentous cytoskeletal tracks (MTs or F-actin) in the cell. Members of the kinesin superfamily have a highly conserved motor domain of ~350 amino acid residues, which contains ATPase and MT binding activities, located at the N terminus, C terminus or internally [1,8]. All kinesins bind MTs and perform a variety of force-generating tasks such as movement of chromosomes, vesicles, organelles and RNA protein complexes, spindle formation and elongation, activation of protein kinases, movement of loosely bound rafts of soluble cargo, and MT polymerization and dynamics [5,9,10,11,12,13]

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