Dock stack with multiple folders
The short answer is, no.

You CAN create Aliases of the two folders, then drop them into another folder (which you then drag to the dock) but this only gives you those folders in a dock folder...

BUT... you can have them operate within one folder.. And you might like this option...


create a folder that you'll use to drop into the dock.  
make aliases of both the ~/App folder and the /App folder
drop them in that folder
put it in the dock
right-click on it and mark it as a List.


Now it'll allow you to "spring into" each of those sub folders on the fly....

look at this URL: http://www.macworld.com/article/1160337/dock_access.html