Regulation of ovule initiation by gibberellins and brassinosteroids in tomato and Arabidopsis: two plant species, two molecular mechanisms

Abstract

Ovule primordia formation is a complex developmental process with a strong impact on the production of seeds. In Arabidopsis this process is controlled by a gene network, including components of the signalling pathways of auxin, brassinosteroids (BRs) and cytokinins. Recently, we have shown that gibberellins (GAs) also play an important role in ovule primordia initiation, inhibiting ovule formation in both Arabidopsis and tomato. Here we reveal that BRs also participate in the control of ovule initiation in tomato, by promoting an increase on ovule primordia formation. Moreover, molecular and genetic analyses of the co-regulation by GAs and BRs of the control of ovule initiation indicate that two different mechanisms occur in tomato and Arabidopsis. In tomato, GAs act downstream of BRs. BRs regulate ovule number through the downregulation of GA biosynthesis, which provokes stabilization of DELLA proteins that will finally promote ovule primordia initiation. In contrast, in Arabidopsis both GAs and BRs regulate ovule number independently of the activity levels of the other hormone. Taken together, our data strongly suggest that different molecular mechanisms could operate in different plant species to regulate identical developmental processes even, as for ovule primordia initiation, if the same set of hormones trigger similar responses, adding a new level of complexity.

Asynchrony of ovule primordia initiation in Arabidopsis

“…The triple mutant of CK receptors (cre1-12 ahk2-2 ahk3-3) has reduced ovule number, indicating CK positively regulates ovule development and number (Higuchi et al, 2004;Bencivenga et al, 2012). The mutant of DELLA protein, the negative regulators of GA signaling, produces fruits with fewer seeds than those in wild-type, indicating GA negative regulates ovule number (Gomez et al, 2018;Barro-Trastoy et al, 2020).…”

On the Way to Ovules: The Hormonal Regulation of Ovule Development

“…For instance, the loss-of-function mutants bri1-5 (Huang et al, 2013), bri1-116 (Jia et al, 2020), and the gain-of-function mutant bin2-1 of the BR signaling negative regulator BRASSINOSTEROID-INSENSITIVE 2 (BIN2) (Huang et al, 2013;Jia et al, 2020), have fewer ovules and seeds than wild-type plants. On the contrary, the gain-of-function mutant bzr1-1D of the positive BR signaling regulator BRASSINAZOLE RESISTANT 1 (BRZ1) presents increased ovule and seed number (Huang et al, 2013;Barro-Trastoy et al, 2020). Supporting this, the BR biosynthesis defective mutant det2-1 and brassinazole (a BR biosynthesis inhibitor) treatments decrease ovule number (Huang et al, 2013;Barro-Trastoy et al, 2020), whereas brassinolide (an endogenous natural BR) treatment increases ovule number (Barro-Trastoy et al, 2020).…”

“…On the other hand, AINTEGUMENTA (ANT) is an AP2 TF that positively regulates organ initiation and growth (Elliott et al, 1996;Krizek, 1999;Mizukami and Fischer, 2000), and was closely associated with ovule primordia formation and ovule development (Elliott et al, 1996;Klucher et al, 1996). During the early stages of ovule initiation, ANT is expressed in the placenta and ovule primordia (Elliott et al, 1996;Barro-Trastoy et al, 2020). Moreover, single ant mutations lead to a reduction in ovule number with no concomitant reduction in pistil length (Klucher et al, 1996;Liu et al, 2000;Barro-Trastoy et al, 2020), which results in decreased ovule density.…”

“…During the early stages of ovule initiation, ANT is expressed in the placenta and ovule primordia (Elliott et al, 1996;Barro-Trastoy et al, 2020). Moreover, single ant mutations lead to a reduction in ovule number with no concomitant reduction in pistil length (Klucher et al, 1996;Liu et al, 2000;Barro-Trastoy et al, 2020), which results in decreased ovule density.…”

Closing Gaps and Opening New Avenues during Megasporogenesis of Rice

“…This experimental effort comes at a time when comparative transcriptomic and comparative physiology aiming to identify gene regulatory networks is blooming (Jones and Vandepoele, 2020). As an example, recent studies showed that the hormonal control of early ovule development in Arabidopsis (Arabidopsis thaliana) and Solanum lycopersicum is differentially orchestrated by gibberellins and brassinosteroids (Barro-Trastoy et al, 2020). This has implications for comparative studies between model plants and crops/cereals but also for studies with an evolutionary perspective.…”