Discovery of a body-wide photosensory array that matures in an adult-like animal and mediates eye-brain-independent movement and arousal.
Title | Discovery of a body-wide photosensory array that matures in an adult-like animal and mediates eye-brain-independent movement and arousal. |
Publication Type | Journal Article |
Year of Publication | 2021 |
Authors | Shettigar N, Chakravarthy A, Umashankar S, Lakshmanan V, Palakodeti D, Gulyani A |
Journal | Proc Natl Acad Sci U S A |
Volume | 118 |
Issue | 20 |
Date Published | 2021 May 18 |
ISSN | 1091-6490 |
Abstract | The ability to respond to light has profoundly shaped life. Animals with eyes overwhelmingly rely on their visual circuits for mediating light-induced coordinated movements. Building on previously reported behaviors, we report the discovery of an organized, eye-independent (extraocular), body-wide photosensory framework that allows even a head-removed animal to move like an intact animal. Despite possessing sensitive cerebral eyes and a centralized brain that controls most behaviors, head-removed planarians show acute, coordinated ultraviolet-A (UV-A) aversive phototaxis. We find this eye-brain-independent phototaxis is mediated by two noncanonical rhabdomeric opsins, the first known function for this newly classified opsin-clade. We uncover a unique array of dual-opsin-expressing photoreceptor cells that line the periphery of animal body, are proximal to a body-wide nerve net, and mediate UV-A phototaxis by engaging multiple modes of locomotion. Unlike embryonically developing cerebral eyes that are functional when animals hatch, the body-wide photosensory array matures postembryonically in "adult-like animals." Notably, apart from head-removed phototaxis, the body-wide, extraocular sensory organization also impacts physiology of intact animals. Low-dose UV-A, but not visible light (ocular-stimulus), is able to arouse intact worms that have naturally cycled to an inactive/rest-like state. This wavelength selective, low-light arousal of resting animals is noncanonical-opsin dependent but eye independent. Our discovery of an autonomous, multifunctional, late-maturing, organized body-wide photosensory system establishes a paradigm in sensory biology and evolution of light sensing. |
DOI | 10.1073/pnas.2021426118 |
Alternate Journal | Proc Natl Acad Sci U S A |
PubMed ID | 33941643 |
PubMed Central ID | PMC8157970 |