TheTrans-Acting Short Interfering RNA3 Pathway and NO APICAL MERISTEM Antagonistically Regulate Leaf Margin Development and Lateral Organ Separation, as Revealed by Analysis of anargonaute7/lobed leaflet1Mutant inMedicago truncatula

Chuanen Zhou,Guangmin Xia,Yuhong Tang,Million Tadege,Zeng-Yu Wang,Lu Han,Jiangqi Wen,Xiaofei Cheng,Kirankumar S Mysore,Jin Nakashima,Chunxiang Fu,Junying Ma,Yang Tan

doi:10.1105/tpc.113.117788

Chuanen Zhou, Guangmin Xia + Show 11 more

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https://doi.org/10.1105/tpc.113.117788

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Abstract

Leaf shape elaboration and organ separation are critical for plant morphogenesis. We characterized the developmental roles of lobed leaflet1 by analyzing a recessive mutant in the model legume Medicago truncatula. An ortholog of Arabidopsis thaliana argonaute7 (AGO7), Mt-AGO7/lobed leaflet1, is required for the biogenesis of a trans-acting short interfering RNA (ta-siRNA) to negatively regulate the expression of auxin response factors in M. truncatula. Loss of function in AGO7 results in pleiotropic phenotypes in different organs. The prominent phenotype of the ago7 mutant is lobed leaf margins and more widely spaced lateral organs, suggesting that the trans-acting siRNA3 (TAS3) pathway negatively regulates the formation of boundaries and the separation of lateral organs in M. truncatula. Genetic interaction analysis with the smooth leaf margin1 (slm1) mutant revealed that leaf margin formation is cooperatively regulated by the auxin/SLM1 (ortholog of Arabidopsis PIN-formed1) module, which influences the initiation of leaf margin teeth, and the TAS3 ta-siRNA pathway, which determines the degree of margin indentation. Further investigations showed that the TAS3 ta-siRNA pathway and no apical meristem (ortholog of Arabidopsis cup-shaped cotyledon) antagonistically regulate both leaf margin development and lateral organ separation, and the regulation is partially dependent on the auxin/SLM1 module.

Highlights

New organs are formed from meristems throughout the life cycle of a plant
The local auxin activity gradient generated by the auxin efflux regulator PIN-FORMED1 (PIN1) is one such mechanism that facilitates initiation of organs at the flanks of the shoot apical meristem (SAM)
Four mutant lines showing obvious changes in leaf margins were identified from screening ;10,000 M. truncatula mutants tagged by the transposable element of tobacco (Nicotiana tabacum) cell type1 (Tnt1)

Summary

Introduction

New organs are formed from meristems throughout the life cycle of a plant. Well-organized and regulated cell division and expansion are crucial for the patterning and elaboration of organ primordia, requiring a mechanism for reiterative specification of new boundaries (Aida and Tasaka, 2006; Berger et al, 2009). The local auxin activity gradient generated by the auxin efflux regulator PIN-FORMED1 (PIN1) is one such mechanism that facilitates initiation of organs at the flanks of the shoot apical meristem (SAM). The auxin accumulation pattern regulated by PIN1 is a prerequisite for the identification of boundaries during organ initiation, the creation of such boundaries requires coordinated actions with other genes such as NAC-domain transcription factor genes (Aida and Tasaka, 2006; Blein et al, 2008; Rast and Simon, 2008; Berger et al, 2009). The first process is the local auxin activity gradient generated by PIN1 (Hay et al, 2006). Two feedback loops involving PIN1 and CUC2 have been conceptualized for the formation of leaf serrations in Arabidopsis (Bilsborough et al, 2011)

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