Arabidopsis TCP4 transcription factor inhibits high temperature-induced homeotic conversion of ovules

The high temperature (HT) caused by globe warming threatens plant survival and food security. How HT affects plant organ identity is largely unknown. Here, we report that Class II TEOSINTE BRANCHED 1/ CYCLOIDEA/ PCF (TCP) transcription factors redundantly protect ovule identity under HT. Disruption of all the Class II TCPs in a duodecuple tcp2/3/4/5/10/13/17/24/1/12/18/16 (tcpDUO) mutant causes HT-induced ovule conversion into carploid structures. Expression of TCP4 in tcpDUO complements the ovule identity conversion under HT. TCP4 interacts with AGAMOUS (AG) and SEPALLATA3 (SEP3) to repress the transactivation activity of AG-SEP3 complex. We further demonstrate that TCP4 interacts with the homeodomain transcription factor BELL1 (BEL1), a key negative regulator inhibiting AG-SEP3 function. BEL1 is degraded via 26S proteasome under HT, while TCP4 represses the degradation of BEL1, and strengthens the association of BEL1 with AG-SEP3. The tcpDUO mutant synergistically interacts with bel1 and seedstick (stk) in which the ovule identity gene STK is mutated, as presented by the conversion of all the ovules into carploid structures in the redecuple tcpDUO bel1 and tcpDUO stk mutants. Our findings not only reveal the critical redundant roles of Class II TCPs in maintaining ovule identity under HT, but also shed a new light on the understanding of the molecular mechanisms by which ovule identity is determined by the integration of internal factors and environmental temperature.