Recently duplicated plant heterotrimeric Gα proteins with subtle biochemical differences influence specific outcomes of signal-response coupling

Abstract

Heterotrimeric G-proteins, comprising Gα, Gβ, and Gγ subunits, regulate key signaling processes in eukaryotes. The Gα subunit determines the status of signaling by switching between inactive GDP-bound and active GTP-bound forms. Unlike animal systems, in which multiple Gα proteins with variable biochemical properties exist, plants have fewer, highly similar Gα subunits that have resulted from recent genome duplications. These proteins exhibit subtle differences in their GTP-binding, GDP/GTP-exchange, and GTP-hydrolysis activities, but the extent to which these differences contribute to affect plant signaling and development remains unknown. To evaluate this, we expressed native and engineered Gα proteins from soybean in an Arabidopsis Gα-null background and studied their effects on modulating a range of developmental and hormonal signaling phenotypes. Our results indicated that inherent biochemical differences in these highly similar Gα proteins are biologically relevant, and some proteins are more flexible than others in influencing the outcomes of specific signals. These observations suggest that alterations in the rate of the G-protein cycle itself may contribute to the specificity of response regulation in plants by affecting the duration of active signaling and/or by the formation of distinct protein-protein complexes. In species such as Arabidopsis having a single canonical Gα, this rate could be affected by regulatory proteins in the presence of specific signals, whereas in plants with multiple Gα proteins, an even more complex regulation may exist, which likely contributes to the specificity of signal-response coupling.