Chlamydomonas PKD2 organizes mastigonemes, hair-like glycoprotein polymers on cilia

Abstract

Mutations in the channel protein PKD2 cause autosomal dominant polycystic kidney disease, but the function of PKD2 in cilia remains unclear. Here, we show that PKD2 targets and anchors mastigonemes, filamentous polymers of the glycoprotein MST1, to the extracellular surface of Chlamydomonas cilia. PKD2–mastigoneme complexes physically connect to the axonemal doublets 4 and 8, positioning them perpendicular to the plane of ciliary beating. pkd2 mutant cilia lack mastigonemes, and mutant cells swim with reduced velocity, indicating a motility-related function of the PKD2–mastigoneme complex. Association with both the axoneme and extracellular structures supports a mechanosensory role of Chlamydomonas PKD2. We propose that PKD2–mastigoneme arrays, on opposing sides of the cilium, could perceive forces during ciliary beating and transfer these signals to locally regulate the response of the axoneme.

Origins of eukaryotic excitability

“…These may be localized to cilia and flagella, which display an active load response [ 137 , 138 ]. Hair-like extensions of cilia (mastigonemes) are also implicated in mechanosensing in Chlamydomonas [ 139 ]. A combination of rheosensing and chemosensing guides sperm motility through the mammalian oviduct.…”

Flagella Ca2+elevations regulate pausing of retrograde intraflagellar transport trains in adherentChlamydomonasflagella

“…Chlamydomonas PKD2 localises to the flagella membrane, but is also bound to the axoneme and to extracellular glycoprotein polymers known as mastigonemes that resemble hair-like appendages along the distal regions of the flagella 49,50 . The tethering of PKD2 to mastigonemes and the axoneme supports a mechanosensory role in Chlamydomonas 50 .…”

“…can occur within seconds even within individual cells 22 . The pkd2 mutants' lack of mastigonemes, indicates that ion channel mutants may influence the arrangement of flagella glycoproteins 50 . Whilst mastigonemes are not thought to be involved in microsphere movements or gliding motility 51,52 , it is clear that knockout of an ion channel could influence the processes that trigger [Ca 2+ ]fla elevations (i.e.…”

Fission yeast polycystin Pkd2p promotes the cell expansion and antagonizes the Hippo pathway SIN

“…Electrophysiological and structural studies have revealed that most polycystins are calcium-permissive cation channels closely associated with the primary cilium (Gonzalez-Perrett et al, 2001; Hanaoka et al, 2000; Liu et al, 2018; Su et al, 2018), but their functions have turned out to be surprisingly diverse. While the fruit fly and worm polycystins are essential for the male fertility (Barr and Sternberg, 1999; Watnick et al, 2003), it plays a non-essential structural role in the cilium of green algae Chlamydomonas reinhardtii (Huang et al, 2007; Liu et al, 2020; Wood et al, 2012). In comparison, the polycystin homologue of social amoebae Dictyostelium discoideum contributes to cell locomotion (Lima et al, 2014).…”

“…However, their functions have turned out to be surprisingly diverse. While the fruit fly and worm polycystins are essential for male fertility (Barr and Sternberg, 1999; Watnick et al, 2003), the polycystin of the green algae Chlamydomonas reinhardtii plays a non-essential structural role in the cilia (Huang et al, 2007; Liu et al, 2020; Wood et al, 2012). In comparison, the polycystin homologue of social amoebae Dictyostelium discoideum contributes to cell locomotion (Lima et al, 2014).…”