Rooney had given England a 29th-minute lead with a superb goal in Moscow's Luzhniki Stadium, but the striker was controversially adjudged to have fouled Konstantin Zyrianov in the box on 69 minutes - and substitute Roman Pavlyuchenko put away the resulting penalty.

And just four minutes later, Pavlyuchenko stole in to score again from close range after Paul Robinson had parried a Zyrianov shot into his path.

The result means Russia have now gained the initiative in Group E - and England will have to hope Guus Hiddink's side slip up in Israel next month.

In the first half, there had been a scare for England after 11 minutes when Aleksandr Kerzhakov went down in the box under a challenge from Joe Cole - but replays showed the Sevilla forward had dived.

Centre-back Vasili Berezutsky became the first player booked on 14 minutes for a late tackle on Cole.

England won their first corner shortly afterwards, and it ended in a Joleon Lescott header being tipped over the bar.

Soon after at the other end, full debutant Lescott and Ferdinand both made crucial blocks from two Russia shots, the second from Bilyaletdinov a real threat to Paul Robinson's goal.

Then on 26 minutes, Konstantin Zurianov's fizzing low shot from just inside the England area was tipped onto the post and wide for a corner by Robinson.

But England took the lead when Michael Owen leaped highest to flick on a long clearance from Micah Richards. Rooney expertly controlled the ball on his chest before smashing it past home goalkeeper Vladmir Gabulov into the centre of the goal.

After Rooney's goal, the home side started to exert considerable pressure and in the space of five minutes forced half-a-dozen corners.

Rooney required treatment on a leg injury soon after the restart but was soon back on the pitch, and on 50 minutes captain Steven Gerrard missed a gilt-edged opportunity to double England's lead.

Gareth Barry swung over a high free-kick from wide on the right, all the way over to an unmarked Gerrard at the far post - but his central midfield colleague sidefooted it just past the post when he should have scored.

Rio Ferdinand picked up a booking on 57 minutes for hauling down Zhirkov, and will now miss England's final qualifier at home to Croatia next month.

The pressure was increasing from the home side - and after 69 minutes, Pavluchenko equalised from the penalty spot.

Rooney tugged at the shirt of Zurianov, and Spanish referee Luis Medina Cantalejo pointed to the penalty spot - though replays showed the offence was committed outside the area.

And with 17 minutes remaining, Pavlyuchenko turned the game on its head by scoring for the second time in four minutes.

Robinson parried away a rising shot from Alexei Berezutsky and the substitute reacted quickest to the rebound.

Steve McClaren responded by bringing on Frank Lampard, Stewart Downing and Peter Crouch in place of Wright-Phillips, Lescott and Joe Cole.

Rooney had a low shot turned around the post by Gabulov and Campbell headed over from a Barry corner - but Russia ran out winners.

Afterwards England boss Steve McClaren rounded on the referee after seeing his side suffer a potentially fatal blow.

"We had it. It was in our grasp and we've ended up losing it," McClaren said.

"I've just seen the penalty again. It's an absolute disgrace .

"It's outside the box. The linesman didn't give it. It was the referee from quite some distance. Things like that turn games.

"We were comfortable. They were running out of ideas and that just turned the game.

"It was a mad four minutes after that and unfortunately we conceded a second.

"But I can't fault the players for the gameplan, the way they've endeavoured to work, the commitment, the blocks we got in, the headers."

"We've ended up losing a game that really, after 70 minutes, I never thought we'd lose."