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After Mr Poots was forced out just three weeks after becoming leader, influential DUP sources told The Telegraph his successor would be expected to ratchet up pressure on Boris Johnson to protect Northern Ireland’s place in the UK.
While no candidate is yet to declare, there are growing calls among MPs and assembly members for the next leader to effectively put the power-sharing agreement on the line unless the Government acts.
A replacement for Mr Poots is expected to be elected by the end of the month, with Sir Jeffrey Donaldson, the DUP’s Westminster leader who ran against him, widely tipped as the favourite.
Mr Poots was forced out on Thursday after signing up to a deal with Sinn Fein, brokered by Brandon Lewis, the Northern Ireland Secretary, to ensure that the Stormont Assembly continued to function.
Mr Lewis was forced to step in after Sinn Fein threatened to collapse the executive over Mr Poots’s decision to nominate Paul Givan, one of his former advisers, as the new first minister.
Sinn Fein had objected to Mr Givan’s appointment due to concerns it would lead to legislation protecting the Irish language being delayed.
To break the deadlock, Mr Lewis promised that Westminster would implement the legislation if required by the end of September.
However, Mr Poots's decision to agree to these terms infuriated many in his party, who demanded he postpone making Mr Givan first minister.
When he defied this request, he was ousted. While Mr Givan remains in place for now, party figures expect he could also be forced out when the next leader is elected.
Thursday night’s chaos now threatens to unleash further instability, with senior DUP figures insisting that the next leader must push back against the terms of the agreement brokered by Mr Lewis.
One source said they expected the next leader to “call the Government’s bluff” and demand clear guarantees that the protocol, which was established to prevent a hard Irish border, is either scrapped or significantly altered.
Since its implementation in January, the protocol, which requires the province to conduct EU border and customs checks, has caused significant trade disruption between Britain and Northern Ireland and has been blamed for fuelling unrest among loyalists.
A DUP MP added on Friday night: “There has got to be an end to this interference in devolution by the Government. They did it with abortion, they did it with the protocol, now they move to take away devolution powers with respect to Irish language at the behest of Sinn Fein.
“The Government is prepared to risk the ire of unionists to do that. When you consider the Government has moved heaven and earth to try to get Sinn Fein in the executive again, I'll look forward to seeing whether they will do the same for unionists.”
The row centres on the New Deal, New Approach agreement which was signed last year in order to restore the Stormont Assembly after a three-year hiatus.
While the deal contains commitments to implementing the Irish language legislation, DUP figures say it also contains “black and white” commitments to providing “unfettered access” to the UK internal market.
On Friday night, the Loyalist Communities Council, the umbrella group which represents unionist paramilitaries, called for the next DUP leader to "stop the constant flow of concessions to Sinn Fein even if that means suspending the normal operation of devolution".
In a statement, it added: "HM Government must retract their ill-thought out and rushed decision to legislate for Irish language at Westminster or risk prompting significant political and community instability."