Sugar availability suppresses the auxin-induced strigolactone pathway to promote bud outgrowth

Abstract

+33 (0)2 41 22 56 32 2 SUMMARY• Apical dominance occurs when the growing shoot tip inhibits the outgrowth of axillary buds. Apically-derived auxin in the nodal stem indirectly inhibits bud outgrowth via cytokinins and strigolactones. Recently, sugar deprivation was found to contribute to this phenomenon.• Using rose and pea, we investigated whether sugar availability interacts with auxin in bud outgrowth control, and the role of cytokinins and strigolactones, in vitro and in planta.• We show that sucrose antagonizes auxin's effect on bud outgrowth, in a dosedependent and coupled manner. Sucrose also suppresses strigolactone-inhibition of outgrowth, and rms3 strigolactone-perception mutant is less affected by reducing sucrose supply; however, sucrose does not interfere with the regulation of cytokinin levels by auxin, and stimulates outgrowth even with optimal cytokinin supply. These observations were assembled into a computational model where sucrose represses bud response to strigolactones, largely independently of cytokinin levels. It quantitatively captures our observed dose-dependent sucrose-hormones effects on bud outgrowth, and allows us to express outgrowth response to various combinations of auxin and sucrose levels as a simple quantitative law.• This study places sugars in the bud outgrowth regulatory network, and paves the way for better understanding of branching plasticity in response to environmental and genotypic factors.Versailles, France) for providing the seeds of Pisum sativum and GR24. We thank the Environment and Agronomy department of INRA for financial support.

Sucrose promotes D53 accumulation and tillering in rice

“…Sucrose has been shown to promote axillary bud outgrowth and alleviate the inhibitory effect of SL during this process in dicotyledonous models 21,26 . However, this antagonistic interaction has not been reported in monocotyledons plants, which have an architecture different compared with eudicots.…”

“…In this species, decapitation triggers bud outgrowth through redistribution of sugars towards axillary buds, and sucrose feeding can trigger bud release 7,8 . To explore whether a similar mechanism for sucrose regulation of gene expression may occur in pea, we examined the expression of PsD3 and PsD14 in pea as well as their downstream target BRC1 , the orthologue of TB1 8,25,26 in response to sucrose feeding and decapitation. Similar to the result observed for D3 in rice in response to sucrose, decapitation led to a decrease in PsD3 and BRC1 expression but not in PsD14 (Figure 7a-c).…”

“…The interaction between sugars and hormones during the control of bud outgrowth is not clear. Recent literature highlights that sucrose can antagonise the effect of auxin by inhibiting SL perception to promote bud outgrowth 26 and that the involvement of cytokinins may be limited to the conditions under which sugars are not readily available 15,25,26 . However, no studies have ever attempted to explore how sucrose and SL interact at the molecular level.…”

Sucrose promotes etiolated stem branching through activation of cytokinin accumulation followed by vacuolar invertase activity

“…Using an elegant set of experiments, Mason et al (2014) demonstrated the systemic movement of sucrose as a branching signal from the leaf to the lateral bud after decapitation. Barbier et al (2015a) demonstrated that sugar availability, together with auxin (Bertheloot et al, 2019), control the entrance of buds into sustained growth. Recently, we showed that sucrose and its hydrolytic products can induce stem branching in a dose-responsive manner under etiolated conditions (Salam et al, 2017).…”

“…Sucrose has been reported to strongly induce CK synthesis in in vitro -grown single nodes of rose in absence of auxin, suggesting that CKs might mediate the effect of sucrose, although the authors concluded that CKs alone are not sufficient to stimulate bud outgrowth in Rosa single nodes (F. Barbier et al, 2015). In presence of auxin in the growth medium, sucrose could not promote CK accumulation, and the CK content did not correlate with the onset of bud outgrowth (Bertheloot et al, 2019). Here, we report here that CKs play an important role in mediating sucrose-promoted bud outgrowth in etiolated potato stem.…”