Babo1, formerly Vop1 and Cop1/2, is no eyespot photoreceptor but a basal body protein illuminating cell division in Volvox carteri

Abstract

In photosynthetic organisms many processes are light dependent and sensing of light requires light-sensitive proteins. The supposed eyespot photoreceptor protein Babo1 (formerly Vop1) has previously been classified as an opsin due to the capacity for binding retinal. Here, we analyze Babo1 and provide evidence that it is no opsin. Due to the localization at the basal bodies, the former Vop1 and Cop1/2 proteins were renamed V.c. Babo1 and C.r. Babo1. We reveal a large family of more than 60 Babo1-related proteins from a wide range of species. The detailed subcellular localization of fluorescence-tagged Babo1 shows that it accumulates at the basal apparatus. More precisely, it is located predominantly at the basal bodies and to a lesser extent at the four strands of rootlet microtubules. We trace Babo1 during basal body separation and cell division. Dynamic structural rearrangements of Babo1 particularly occur right before the first cell division. In four-celled embryos Babo1 was exclusively found at the oldest basal bodies of the embryo and on the corresponding d-roots. The unequal distribution of Babo1 in four-celled embryos could be an integral part of a geometrical system in early embryogenesis, which establishes the anterior-posterior polarity and influences the spatial arrangement of all embryonic structures and characteristics. Due to its retinal-binding capacity, Babo1 could also be responsible for the unequal distribution of retinoids, knowing that such concentration gradients of retinoids can be essential for the correct patterning during embryogenesis of more complex organisms. Thus, our findings push the Babo1 research in another direction.

Molecular and cellular dynamics of early embryonic cell divisions inVolvox carteri

“…H, Same as in G but with additional indication of the position of basal bodies/centrioles and microtubular rootlets. The older basal body/centriole and the proximal parts of the rootlet microtubules are located by overlaying an image that resolves the localization of YFP-tagged basal body protein Babo1 (Babo1:YFP in orange hot) ( von der Heyde and Hallmann, 2020 ). The position of younger basal bodies/centrioles (empty circles) and four-membered rootlet microtubules (dashed lines) was estimated based on earlier publications ( Holmes and Dutcher, 1989 ; Kirk et al, 1991 ; Ehler et al, 1995 ).…”

“…In prophase, the duplicated centrosomes are spatially separated and positioned for spindle formation ( Figures 6F and 12B ). The process is guided by the microtubular rootlets, as shown in both Chlamydomonas and Volvox ( Holmes and Dutcher, 1989 ; von der Heyde and Hallmann, 2020 ). According to results in C. reinhardtii , the two-membered rootlets provide orientation, whereas the four-membered rootlets connect the two pairs of centrioles ( Doonan and Grief, 1987 ; Segaar and Gerritsen, 1989 ; Gaffal and el-Gammal, 1990 ).…”

“…AAZ65844) ( Kremers et al, 2006 ). The yfp gene version used was previously engineered to match the codon usage of C. reinhardtii ( Lauersen et al, 2015 ) but it is also suitable for use in V. carteri ( Tian et al, 2018 ; von der Heyde and Hallmann, 2020 ). For visualization of cell nuclei, YFP was tagged with a minimal nuclear targeting sequence using the NLS of simian virus 40 (PKKKRKV) ( Kalderon et al, 1984 ).…”

An engineered membrane-bound guanylyl cyclase with light-switchable activity

“…However, until now, only three rhodopsin molecules are functionally characterized [6][7][8] and two of them with confirmed physiological function [9]. The first hypothesized "opsins," Chlamyopsin-1 and 2 (Cop1, Cop2) [10], show no homology to the other authentic Chlamydomonas opsins and are not transmembrane proteins [8,11] and therefore should not be regarded as "opsins." Their Volvox carteri homolog Vop1 was exclusively found at the oldest basal bodies of the embryo and on the corresponding d-roots and was renamed "basal body protein-1" (Babo1 [11]).…”

“…The first hypothesized "opsins," Chlamyopsin-1 and 2 (Cop1, Cop2) [10], show no homology to the other authentic Chlamydomonas opsins and are not transmembrane proteins [8,11] and therefore should not be regarded as "opsins." Their Volvox carteri homolog Vop1 was exclusively found at the oldest basal bodies of the embryo and on the corresponding d-roots and was renamed "basal body protein-1" (Babo1 [11]). Cop3 and Cop4 (originally named CSRA and CSRB for "Chlamydomonas Sensory Rhodopsins A and B") were the first two authentic Chlamydomonas opsins, shown to function physiologically as phototaxis receptors of C. reinhardtii [9].…”