I had this issue once, on Qubes 3.2. a couple of months back.
It happened when I accidentally filled my laptops drive space, and it corrupted a couple of configuration files, especially those of Xfce4. I had to re-do every configuration changes I had made as they had become default, as if it was a clean install. Thing is, some didn't just default, they broke. For example I lost all my dom0 System Tools, dom0 terminal, and so forth.
This seems a bit similar to your situation? when you installed that template, did you happen to hit your drives max capacity? This is something that could easily be imagined to have happened if you made a large install such as an template. It may also have shrunk again after a reboot, so unless you got plenty of drive space, this is a likely cause.
Also it seems it won't behave the same way every time this happens, so the symptoms may vary when hitting the max drive capacity.
Either way, I thought it was too much trouble to work it out, and I had to re-install Qubes anyway, so I just went ahead and took a backup and re-installed. At any rate, it may be faster than solving it too, for you as well.