Progress in understanding the role of auxin in lateral organ development in plants

doi:10.1016/j.pbi.2019.10.007

Current Opinion in Plant Biology

Volume 53, February 2020, Pages 73-79

https://doi.org/10.1016/j.pbi.2019.10.007 Get rights and content

Plants continuously produce lateral organs from the shoot apex such as leaves and flowers, providing an excellent opportunity to study their development. The plant hormone auxin plays a central role in this process by promoting organ formation where it accumulates due to polar auxin transport. Recently, the use of live-imaging, fine perturbation techniques and computational modelling has helped researchers make exciting progress in addressing long-standing questions on plant organogenesis, not only regarding the role of auxin in promoting growth but also on the regulation of morphogenesis and transcriptional control. In this review, we discuss a number of recent studies that address these points, with particular reference to how auxin acts in early leaf development and in leaf shape.

Introduction

Leaves and flowers initiate on the flanks of the shoot meristem, with successive leaves arising in the position of an auxin maximum [1,2]. In turn, the localized maxima are positioned by the auxin efflux carrier PIN1, which directs auxin towards initiation sites according to a feedback loop between auxin signalling and PIN1 polarity [1,3]. However, while auxin can induce organ growth on the flanks of the meristem, tissues at the apex or further down the flank are non-responsive [2]. What defines the auxin responsive peripheral zone? What does auxin actually do to promote tissue outgrowth and how is the shape of the resulting organ controlled? Below we discuss several recent studies that address these questions.

Section snippets

Adaxial-abaxial patterning and organ positioning: several models

Leaves initiate in the peripheral region of the shoot apical meristem (SAM) and establish along three axes: an adaxial-abaxial (top to bottom), proximal-distal (base to tip) and mediolateral (middle to margin). The adaxial-abaxial axis forms two opposing sides of the leaf primordium, which differentiate into distinct tissues and both tissues are required for lamina development [4, 5, 6]. The tissues closest to the shoot axis are called adaxial while the tissues further away are called abaxial.

Downstream of auxin

Which genes apart from WOX1 and PRS are known to act downstream of auxin to promote organ growth? Several transcription factors are induced by auxin at primordial positions via Auxin Response Factor 5 (ARF5)/MONOPTEROS (MP) and function to promote flower development, through induction of genes including LEAFY, AINTEGUMENTA, AINTEGUMENTA-LIKE6 and FILAMENTOUS FLOWER (FIL) [22,23]. More recently, the LEAFLESS (LFS) gene from tomato, encoding a gene closely related to the Arabidopsis DORNRONSCHEN (

Leaf morphogenesis

So far, we have discussed recent work focused on genetic regulatory networks which pattern cell types and regulate and are regulated by auxin. But how does auxin function at a cellular level to promote organ outgrowth and how is the shape of new organs determined? Recent work has provided important new insights into both these questions. Previous work has shown that auxin acts to promote organ formation at least in part through the local de-polymerization of microtubules. Since interphase

Conclusion

It is an exciting time for understanding plant organ development. The work discussed here represents significant progress in addressing questions that have been highlighted in the field for decades, facilitated by the use of quantitative live-imaging and modelling. Nevertheless, several findings remain under dispute and it will be important to resolve these disagreements in order to make further progress and achieve a cohesive understanding across the field. In addition to the studies cited

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgement

Funding is gratefully acknowledged by MH from the Australian Research Council (DP180101149).

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Progress in understanding the role of auxin in lateral organ development in plants

Introduction

Section snippets

Adaxial-abaxial patterning and organ positioning: several models

Downstream of auxin

Leaf morphogenesis

Conclusion

Conflict of interest statement

References and recommended reading

Acknowledgement

Curr Biol

Curr Biol

Proc Natl Acad Sci U S A

bioRxiv

Curr Biol

Science

Development

Nat Plants

Nat Genet

Regulation of phyllotaxis by polar auxin transport

Nature

Auxin regulates the initiation and radial position of plant lateral organs

Plant Cell

Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots

Nature

Phantastica - a gene required for dorsoventrality of leaves in Antirrhinum-Majus

Development

The Sussex signal: insights into leaf dorsiventrality

Development

Morphogenesis in Solanum tuberosum I: experimental investigation of leaf dorsiventrality and orientation in the juvenile shoot

Phytomorphology

Cell type boundaries organize plant development

eLife

Dynamic patterns of gene expression during leaf initiation

J Genet Genomics

Spatial auxin signaling controls leaf flattening in Arabidopsis

Curr Biol

Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems

eLife

Quantitative analysis of auxin sensing in leaf primordia argues against proposed role in regulating leaf dorsoventrality

eLife

The 35S promoter-driven mDII auxin control sensor is uniformly distributed in leaf primordia

J Integr Plant Biol

Plant small RNAs as morphogens

Curr Opin Cell Biol