4.7 Article

Auxin biosynthesis and cellular efflux act together to regulate leaf vein patterning

Journal

JOURNAL OF EXPERIMENTAL BOTANY
Volume 72, Issue 4, Pages 1151-1165

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/jxb/eraa501

Keywords

Auxin; auxin biosynthesis; auxin canalization; auxin transport; leaf; mathematical modeling; vein patterning

Categories

Funding

  1. Baden-Wurttemberg Stiftung
  2. Deutsche Forschungsgemeinschaft [SFB 746]
  3. Excellence Initiative of the German Federal Government [EXC 294]
  4. Excellence Initiative of the German State Government [EXC 294]
  5. Bundesministerium fur Forschung und Technik (BMBF SYSTEC, PROBIOPA, MICROSYSTEMS)
  6. Deutsches Zentrum fur Luft und Raumfahrt [DLR 50WB1022]
  7. Freiburg Initiative for Systems Biology
  8. European Union Framework 6 Program (AUTOSCREEN) [LSHG-CT-2007-037897]
  9. National Science Foundation (USA)
  10. Japan Society for the Promotion of Science KAKENHI [24570047, 16K07396]
  11. Burroughs Wellcome Fund
  12. Grants-in-Aid for Scientific Research [16K07396, 24570047] Funding Source: KAKEN

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This study reveals a synergistic relationship between auxin biosynthesis and cellular auxin efflux in leaf vein development, explaining the formation of midvein morphology through computational modeling. The findings suggest that the site-specific accumulation of auxin, regulated by the balanced action of cellular auxin efflux and local auxin biosynthesis, is crucial for leaf vein formation.
Our current understanding of vein development in leaves is based on canalization of the plant hormone auxin into self-reinforcing streams which determine the sites of vascular cell differentiation. By comparison, how auxin biosynthesis affects leaf vein patterning is less well understood. Here, after observing that inhibiting polar auxin transport rescues the sparse leaf vein phenotype in auxin biosynthesis mutants, we propose that the processes of auxin biosynthesis and cellular auxin efflux work in concert during vein development. By using computational modeling, we show that localized auxin maxima are able to interact with mechanical forces generated by the morphological constraints which are imposed during early primordium development. This interaction is able to explain four fundamental characteristics of midvein morphology in a growing leaf: (i) distal cell division; (ii) coordinated cell elongation; (iii) a midvein positioned in the center of the primordium; and (iv) a midvein which is distally branched. Domains of auxin biosynthetic enzyme expression are not positioned by auxin canalization, as they are observed before auxin efflux proteins polarize. This suggests that the site-specific accumulation of auxin, as regulated by the balanced action of cellular auxin efflux and local auxin biosynthesis, is crucial for leaf vein formation.

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