I believe you need like 14GB/s+ for 4k. That's why TB(thunderBolt)3 will be the true update to TB. TB1 and TB2 are both 20GB/s connections. TB1 was 2 10GB/s with TB2 combined the two into one 20GB/s lane. TB Display uses about 7GB/s by itself. Since TB1 is limited to 10GB/s per lane you can't push thought enough data to run a 4K monitor. That's not taking into account you graphic card limits.
That's one of the reasons I'm waiting to upgrade my Macbook Pro early 2011. I'll either get a Mac Pro or wait until 2015 when TB3 is to come out. That and I have to save up for it.
Most of the 4K displays on the market at the moment can be driven at 60 Hz by using multiple inputs. OG Thunderbolt can carry two DisplayPort 1.1a main links, each capable of driving one of the 1920 x 2160 tiles in the current crop of tiled displays. This is kludgey at best with the Dell displays (it only works in Picture by Picture mode) and not possible with the ASUS PQ321QE (the EMEA version of the PQ321Q which only has a single input). If you have two Thunderbolt ports, you can use a pair of relatively inexpensive mini DisplayPort to high-speed HDMI adapters and two high-speed HDMI cables. If you only have a single available Thunderbolt port, the cheapest way thus far to break out both display streams is to daisy chain a couple Thunderbolt docks with high-speed HDMI outputs, which is none to cheap starting at $392, but does additionally provide 6x USB 3.0 and 2x GbE ports at least.
As you pointed out though, the GPU [edit: and even moreso the drivers] are often the limiting factor right now.
TB2 may in theory have 20Gb/s bandwidth. But unfortunately all Intel TB2 controller uses x4 PCIe 2.0 interface which has already close to max out at 4k @ 60hz resolution. Any higher resolution, higher refresh rate, or higher color bit rate seems to be impossible. x4 PCIe 3.0 interface will double the bandwidth but that's probably we are talking about the next generation of hardware.
Thunderbolt controllers also have DisplayPort sink and source connections as well; DisplayPort packets are never transported over PCIe. OG Thunderbolt can transport up to two DisplayPort 1.1a HBR1 main links, which top out at 8.64 Gbit/s, since it provides 2x 10 Gbit/s channels per port. Thunderbolt 2 supports up to two DP 1.2 sink connections, and can transport either 2x HBR1 main links or 1x HBR2 main link over a pair of bonded 10 Gbit/s channels.
If TB1 has a limit of 20GBPS and one TB Display uses 7GB, then how are people running a triple TB display setup on TB 1? Just curious.
While you can only drive up to 2 external displays using OG Thunderbolt, there's a good chance you can also drive a built in panel (or an HDMI connected display on some Mac minis) for 3, or use the HDMI port on a MacBook Pro (Retina, 15-inch) with discrete graphics for 4. I think many of the people complaining about the issues with 10.9.3 and more than 2 displays are using Mac Pros (Late 2013), and most of them appear to be using multiple DP to other adapters (this is merely an observation of correlation and may have nothing to do with the cause of the problem).
4K @ 60Hz is 12Gbps. 5K on the other hand is around 22 Gbps, TB2 won't be enough. But if TB3 arrives next year, then Apple may wait and ship a 5K display without doing any 4K one. I doubt they would offer a 4K and a 5K together and I don't think they really want to mess up the UI scaling at this point.
Thunderbolt is just a transport layer used to carry DisplayPort and PCIe packets and has no bearing on display connectivity standards. Any display requiring more than 17.28 Gbit/s (the limit of DisplayPort 1.2 HBR2) will require multiple links or DisplayPort 1.3. Since virtually all of the 4K panels on the market at the moment use TCONs with LVDS, V-by-One, or HBR1 eDP interfaces, they all present the display surface as two tiles, each requiring its own input. The only way to drive the whole shebang at 60 Hz with a single cable is to use DisplayPort 1.2 Multi Stream Transport along with an MST hub embedded in the display which separates the streams for each tile and passes them to the TCON. A tiled 5K display can be driven today, but would require two links using DP HBR2 or 4 with conventional TCONs. For the panels built into the iMacs, that really wouldn't be a problem, as long as the GPU can support a sufficient number of display streams (Intel HD Graphics currently only supports 3, NVIDIA can manage 4, and AMD bumps it up to 6).
You can't effectively displace 27" with a 4K 21". 24" is probably the smallest practical size for the top imac.
AUO has a 27" 3840 x 2160 panel with an eDP interface due to ramp in Q3 of this year. That sounds to me like a likely candidate for an Apple 4K Thunderbolt Display, but I don't see a clear path for the iMacs at this point.
WTF does Apple need to "officially support" every stinking monitor being manufactured? That could get really ugly really fast trying to depend on Apple to release new drivers all the time when they cannot even keep their regular video drivers and 3D system up-to-date in a timely fashion. There should be a STANDARD that all 4k monitors support and Apple should then just support that standard, not this piece meal one-at-a-time approach.
That STANDARD is VESA DisplayID 1.3, which was only finalized less than 2 weeks before Mavericks was released and well after the majority of the currently available 4K, 60 Hz displays began shipping. I'm sure we'll get there, but at the moment, people just want to know if display "x" is supported. By my count there are only 8 4K displays capable of 60 Hz operation available for less than $15K, so Apple's approach isn't entirely unreasonable. Once the displays are are actually standardized, Apple can try to make sure their drivers support that standard.
Additional info:
Comparison of known 4K LCD panels
Comparison of 4K displays that support 60 Hz operation
List of display bandwidth requirements based on CVT-R