Phyllotaxis involves auxin drainage through leaf primordia

Abstract

The spatial arrangement of leaves and flowers around the stem, known as phyllotaxis, is controlled by an auxin-dependent reiterative mechanism that leads to regular spacing of the organs and thereby to remarkably precise phyllotactic patterns. The mechanism is based on the active cellular transport of the phytohormone auxin by cellular influx and efflux carriers, such as AUX1 and PIN1. Their important role in phyllotaxis is evident from mutant phenotypes, but their exact roles in space and time are difficult to address due to the strong pleiotropic phenotypes of most mutants in phyllotaxis. Models of phyllotaxis invoke the accumulation of auxin at leaf initials and removal of auxin through their developing vascular strand, the midvein. We have developed a precise microsurgical tool to ablate the midvein at high spatial and temporal resolution in order to test its function in leaf formation and phyllotaxis. Using amplified femtosecond laser pulses, we ablated the internal tissues in young leaf primordia of tomato (Solanum lycopersicum) without damaging the overlying L 1 and L 2 layers. Our results show that ablation of the future midvein leads to a transient accumulation of auxin in the primordia and to an increase in their width. Phyllotaxis was transiently affected after midvein ablations, but readjusted after two plastochrons. These results indicate that the developing midvein is involved in the basipetal transport of auxin through young primordia, which contributes to phyllotactic spacing and stability.

Self-organizing periodicity in development: organ positioning in plants

“…Underneath the epidermis, there was no evidence of auxin transport channels oriented internally, unlike in the wild type, which is consistent with the known role of MP in promoting the formation of vascular tissue (Przemeck et al, 1996). One hypothesis supported by computer simulations and suggested by previous laser ablation experiments (Deb et al, 2015) is that the shifting of auxin peaks and PIN1 polarity patterns is due to excessive auxin build-up that arises because of the lack of auxin transport to internal tissues (Bhatia et al, 2016). However, the fact that neither PIN1 nor auxin influx carrier activity is required below the epidermis for normal phyllotaxis argues against an auxin transport-related problem (Kierzkowski et al, 2013), suggesting that other auxinregulated factors must be required sub-epidermally to anchor PIN1 polarity convergence patterns in the epidermis.…”

Vein Patterning by Tissue-Specific Auxin Transport

“…Alternatively, patterning of local epidermal features, such as peaks of auxin production or response, and of the processes that depend on those features may be mediated by auxin transport in underlying tissues; there is evidence for such possibility (e.g., (Deb, Marti, Frenz, Kuhlemeier, & Reinhardt, 2015)), and our results are consistent with that evidence. In the future, it will be interesting to test these and other possibilities, but already now our results refute all the vein patterning hypotheses that depend on polar auxin transport from the epidermis.…”

Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis

“…Notably, no evidence of pro-vascular tissue marked by PIN1 was detected (Figure 4M). Because vascular tissues have been associated with auxin depletion [27], we tested whether auxin-triggered auxin depletion could act to stabilize auxin distribution patterns generated by a previously proposed feedback model for auxin transport consistent with our findings [28] (see the Supplemental Experimental Procedures). We found that without negative feedback on auxin concentrations, the auxin maxima generated by this model could easily shift with respect to the underlying cells due to saturation of the transport system, leading to diffusion or “leakage” of auxin laterally [28] (Movie S4).…”