Leaf vein patterning is regulated by the aperture of plasmodesmata intercellular channels

Abstract

To form tissue networks, animal cells migrate and interact through proteins protruding from their plasma membranes. Plant cells can do neither, yet plants form vein networks. How plants do so is unclear, but veins are thought to form by the coordinated action of the polar transport and signal transduction of the plant hormone auxin. However, plants inhibited in both pathways still form veins. Patterning of vascular cells into veins is instead prevented in mutants lacking the function of the GNOM (GN) regulator of auxin transport and signaling, suggesting the existence of at least one more GN-dependent vein-patterning pathway. Here we show that in Arabidopsis such a pathway depends on the movement of auxin or an auxin-dependent signal through plasmodesmata (PDs) intercellular channels. PD permeability is high where veins are forming, lowers between veins and nonvascular tissues, but remains high between vein cells. Impaired ability to regulate PD aperture leads to defects in auxin transport and signaling, ultimately leading to vein patterning defects that are enhanced by inhibition of auxin transport or signaling. GN controls PD aperture regulation, and simultaneous inhibition of auxin signaling, auxin transport, and regulated PD aperture phenocopies null gn mutants. Therefore, veins are patterned by the coordinated action of three GN-dependent pathways: auxin signaling, polar auxin transport, and movement of auxin or an auxin-dependent signal through PDs. Such a mechanism of tissue network formation is unprecedented in multicellular organisms.

Plasmodesmata play a key role in leaf vein patterning

“…How these findings translate to either other plant patterning processes or vein patterning in other species [10] form open and exciting questions for future research. [5] show that in addition to polarised PIN1-mediated auxin transport within vein cell files, open plasmodesmata enable diffusion between adjacent vein cells. Their study reveals that diffusion of an auxin signal through plasmodesmata is essential to leaf vein patterning in Arabidopsis.…”

“…However, until now, the mechanistic basis of vein pattern formation remained elusive, given plants inhibited in both carrier-mediated auxin transport and auxin signalling still form some vein patterns [ 4 ]. In their new study published in PLOS Biology , Linh and Scarpella investigated whether diffusion through plasmodesmata plays a role in vein patterning, revealing this to be an essential component of vein patterning [ 5 ].…”

“…To test whether plasmodesmal diffusion also affects vein patterns, Linh and Scarpella [ 5 ] first modified plasmodesmal aperture using callose synthesis mutants ( cals3-d and gsl8 ); in these mutants, they observed defects in vein patterning, with fewer veins, open loops, vein fragments, and vascular clusters. Linh and Scarpella then considered whether there are spatial and temporal variations in plasmodesmal permeabilities during vein development.…”

“…In summary, Linh and Scarpella [ 5 ] elucidate a key mechanistic component of Sach’s Canalisation hypothesis. Their elegant study demonstrates that regulation of plasmodesmata is essential for vein patterning.…”

“…[5] first modified plasmodesmal aperture using callose synthesis mutants (cals3-d and gsl8); in these mutants, they observed defects in vein patterning, with fewer veins, open loops, vein fragments, and vascular clusters. Linh and Scarpella then considered whether there are spatial a1111111111 Band LR (2022) Plasmodesmata play a key role in leaf vein patterning.…”