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Jayawardene anchored the innings brilliantly to notch up his 27th Test century and his sixth double ton, and found an able partner in Prasanna Jayawardene (84 not out) as the visitors pushed the hosts on the backfoot by reaching a mammoth 591 for five at close on the third day.
It turned out to be a hard grind for the Indians as the Lankans capitalised on a good batting strip at the Motera stadium to consolidate the position on a day which again saw more than 300 runs being scored.
Resuming at the overnight score of 275 for three in reply to India's 426, the islanders lost the wicket of Thilan Samaraweera (70) and Angelo Mathews (17) in the pre-lunch session but the two Jayawardenes put on a marathon undefeated 216-run partnership to put Sri Lanka on course for their first Test triumph on Indian soil.
With two days left and the pitch expected to aid the spinners, the hosts have a daunting task to prevent the tourists from taking a 1-0 lead in the three-match series.
The pressure will be on the Indians and their much touted batting line-up will have to bat out of their skins to draw the match.
With runs coming freely right through the day, Indian captain Mahendra Singh Dhoni was forced to adapt a defensive strategy but it still failed to contain the run flow. Mahela and Prasanna never really looked in any discomfort and went on to create a record sixth wicket partnership, erasing the previous unbeaten record of 189 by Aravinda De Silva and Arjuna Ranatunga against Zimbabwe at Colombo in 1998.
This was only the second time Sri Lanka have taken a first-innings lead in India, and only the first time they have crossed 450 in the country.
In the morning, Jayawardene and Samaraweera, who started at their overnight individual score of 36 and 45 respectively, completed half centuries before the later was brilliantly caught at square leg by a leaping Yuvraj Singh off Ishant Sharma, just 35 minutes before lunch.
The fourth wicket duo, who put on 138 runs in 166 minutes and 250 balls, looked untroubled against the spin duo of Harbhajan Singh and Amit Mishra and completed their half centuries before Dhoni summoned the second new ball.
Off spinner Harbhajan Singh struck just before lunch, dismissing Mathews, caught at short leg by Gautam Gambhir, to bring the Indians back into the contest.
Dhoni's tactic of taking the new ball paid dividends when the 33-year-old Samaraweera, after striking nine fours in his 166-minute innings, pulled a short Ishant delivery to the right of Yuvraj who leapt and completed a tumbling catch.
Although the wicket boosted India's hopes, Jayawardene and Mathews prevented further damage till the last over before lunch.
The 32-year-old Jayawardene, who back cut Harbhajan for the first four of the morning, followed suit ten minutes later by reaching his 36th half century and in the process also bringing up Sri Lanka's 300 in the 75th over.
India asked for the second new ball after 80.1 overs, 35 minutes after play began today but the move did not yield result initially. Despite a leg slip in place, Jayawardene glanced the gangling Sharma for two fours to fine leg.
This resulted in Dhoni's calling back Harbhajan and Mishra just before the lunch. But Mathews welcomed the leg-spinner with a six off a no ball over the long-on boundary and then pulled him disdainfully for a four.
However, Mathews departed in the next over when he stepped out to Harbhajan only to be beaten by the turn and bounce to give a simple catch to short leg's hands, which looked controversial in TV replays.
Jayawardene completed his century soon after the lunch. It was the right-hander's first century in India after failing to achieve the feat on his only previous visit in 2005 despite having scored four half centuries in five innings.
It was also Mahela's ninth century outside home and fifth three-figure knock against India.