Auxin‐mediated lamina growth in tomato leaves is restricted by two parallel mechanisms

Abstract

SUMMARYIn the development of tomato compound leaves, local auxin maxima points, separated by the expression of the Aux/IAA protein SlIAA9/ENTIRE (E), direct the formation of discrete leaflets along the leaf margin. The local auxin maxima promote leaflet initiation, while E acts between leaflets to inhibit auxin response and lamina growth, enabling leaflet separation. Here, we show that a group of auxin response factors (ARFs), which are targeted by miR160, antagonizes auxin response and lamina growth in conjunction with E. In wild-type leaf primordia, the miR160-targeted ARFs SlARF10A and SlARF17 are expressed in leaflets, and SlmiR160 is expressed in provascular tissues. Leaf overexpression of the miR160-targeted ARFs SlARF10A, SlARF10B or SlARF17, led to reduced lamina and increased leaf complexity, and suppressed auxin response in young leaves. In agreement, leaf overexpression of miR160 resulted in simplified leaves due to ectopic lamina growth between leaflets, reminiscent of e leaves. Genetic interactions suggest that E and miR160-targeted ARFs act partially redundantly but are both required for local inhibition of lamina growth between initiating leaflets. These results show that different types of auxin signal antagonists act cooperatively to ensure leaflet separation in tomato leaf margins.

Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha

“…Class C ARFs also promote the formation of shoot meristems in undifferentiated callus by directly repressing negative regulators of cytokinin signalling (Qiao et al ., ; Liu et al ., ). Auxin response reporters have been shown to be both induced and repressed by class C ARF activity in angiosperms, suggesting a contextual role for these genes in development (Mallory et al ., ; Wang et al ., ; Liu et al ., ; Ben‐Gera et al ., ). Irrespective of their function as transcriptional repressors or activators, genetic studies suggest that class C ARFs have the potential to antagonize auxin signalling (Turner et al ., ; Ben‐Gera et al ., ).…”

“…The class C ARF/MIR160 module in angiosperms regulates a range of processes including leaf margin complexity and lamina growth (Mallory et al ., ; Hendelman et al ., ; Ben‐Gera et al ., ), nodule formation in soybean roots (Turner et al ., ; Nizampatnam et al ., ), root meristem patterning (Wang et al ., ; Ding & Friml, ; Bennett et al ., ) floral determinacy (Liu et al ., ), ovary and fruit patterning, floral organ abscission (Damodharan et al ., ) and seed germination (Liu et al ., , ). Class C ARFs also promote the formation of shoot meristems in undifferentiated callus by directly repressing negative regulators of cytokinin signalling (Qiao et al ., ; Liu et al ., ).…”

Tuning of SlARF10A dosage by sly‐miR160a is critical for auxin‐mediated compound leaf and flower development

“…Recently, fine regulation of ARF17 expression by miR160 was suggested to play a role in Arabidopsis tapetum development and pollen wall formation (Wang et al ., ). In situ hybridizations indicated that the expression domains of sly‐miR160 and SlARF10A overlap at the margins of the leaf and leaflet primordia (Hendelman et al ., ; Ben‐Gera et al ., ). In addition, our data demonstrate the high sensitivity of SlARF10A expression to even small changes in sly‐miR160a levels (Figure b).…”

“…SlARF10A has been proposed to function as an auxin‐response inhibitor according to a protoplast assay (Zouine et al ., ). Consistent with this finding, SlARF10A was suggested to be involved in the spatial restriction of the auxin response that drive leaf blade outgrowth (Ben‐Gera et al ., ). Therefore, we concluded that by fine tuning the expression of this repressor ARF, sly‐miR160a promoted auxin‐dependent compound leaf initiation, primary and secondary morphogenesis.…”

“…Constitutive expression of an miR160‐resistant SlARF10A and the upregulation of SlARF10A and SlARF17 due to miR160 knockdown severely inhibited leaflet blade outgrowth (Hendelman et al ., ; Damodharan et al ., ). Conversely, leaf‐specific silencing of SlARF10A and SlARF17 by sly‐miR160 overexpression caused an expanded auxin response in the leaf primordia, extra blade outgrowth and ectopic blade formation on the leaf rachis (Ben‐Gera et al ., ). The above observations suggest that sly‐miR160 promotes auxin‐driven blade outgrowth by negative regulation of the corresponding repressor ARFs expression.…”