Photooligomerization Determines Photosensitivity and Photoreactivity of Plant Cryptochromes

Plant and non-plant species possess cryptochrome (CRY) photoreceptors to mediate blue light regulation of development or the circadian clock. The blue light-dependent homooligomerization of Arabidopsis CRY2 is a known early photoreaction necessary for its functions, but the photobiochemistry and function of light-dependent homooligomerization and heterooligomerization of cryptochromes, collectively referred to as CRY photooligomerization, have not been well established. Here, we show that photooligomerization is an evolutionarily conserved photoreaction characteristic of CRY photoreceptors in plants and some non-plant species. Our analyses of the kinetics of the forward and reverse reactions of photooligomerization of Arabidopsis CRY1 and CRY2 provide a previously unrecognized mechanism underlying the different photosensitivity and photoreactivity of these two closely related photoreceptors. We found that photooligomerization is necessary but not sufficient for the functions of CRY2, implying that CRY photooligomerization is presumably accompanied by additional function-empowering conformational changes. We further demonstrated that the CRY2–CRY1 heterooligomerization plays roles in regulating functions of Arabidopsis CRYs in vivo. Taken together, these results suggest that photooligomerization is an evolutionarily conserved mechanism determining the photosensitivity and photoreactivity of plant CRYs. Photooligomerization of Arabidopsis cryptochromes is fast, fluence rate dependent, and dark reversible, and the photosensitivity of photooligomerization determines the photoreactivity of crytochromes. Photooligomerization is also an evolutionarily conserved photoreaction characteristic of CRY photoreceptors in plants and some non-plant species. Moreover, photooligomerization is necessary but not sufficient for CRY2 functions, and CRY2–CRY1 heterooligomerization plays roles in regulating functions of Arabidopsis CRYs.