SlERF.B1 controls fruit maturity and the transition to ripening by regulating the auxin-ethylene cross-talk through SlIAA2 and SlARF9A in tomato

Abstract

The onset of fruit ripening is a tightly regulated process under complex hormonal control. Although ethylene is essential for promotion of climacteric fruit ripening, its action is dependent on hormones like ABA (a promoter of ripening) and auxin (a ripening inhibitor). SlERF.B1 was identified as an activator type ERF that controls the auxin pathway prior to the onset of ripening. It is up-regulated during fruit growth but down-regulated once fruit attains maturity. Suppression of SlERF.B1 led to an early onset of ripening without altering fruit growth through synchronization of the mature green and breaker stages that are usually spaced apart by 4–5 days. Its over-expression delayed the onset of ripening by two days. Comparative transcriptomic studies showed the earlier activation of the ethylene, lycopene/carotenoid and softening pathway genes in SlERF.B1 suppression lines but delayed expression in over-expression lines. SlERF.B1 manipulation most prominently affected the auxin pathway with genes such as SlGH3.2 and SlDAO (associated with auxin conjugation and degradation) being up-regulated, and components of the auxin signaling machinery (such as Aux/IAAs and ARFs) being down-regulated in suppression lines. SlSAUR69 (which suppresses auxin transport and inhibits auxin responses) and SlARF2A (which promotes ripening) were up-regulated in suppression lines but down-regulated in Oex lines. SlERF.B1 functions through direct binding to the promoters of the auxin signaling components, SlIAA2 and SlARF9, and may regulate fruit maturity and ripening onset by keeping auxin responses high and reducing ethylene responses until the fruit is ready for ripening.