Biphasic regulation of the transcription factor ABORTED MICROSPORES (AMS) is essential for tapetum and pollen development in Arabidopsis.

Alison C Ferguson,Simon Pearce,Ivana Ferjentsikova,Zheng Yuan,Leah R Band,John King,Zoe A Wilson,Dabing Zhang,Caiyun Yang

doi:10.1111/nph.14200

Abstract

Summary Viable pollen is essential for plant reproduction and crop yield. Its production requires coordinated expression at specific stages during anther development, involving early meiosis‐associated events and late pollen wall formation. The ABORTED MICROSPORES (AMS) transcription factor is a master regulator of sporopollenin biosynthesis, secretion and pollen wall formation in Arabidopsis. Here we show that it has complex regulation and additional essential roles earlier in pollen formation.An inducible‐AMS reporter was created for functional rescue, protein expression pattern analysis, and to distinguish between direct and indirect targets. Mathematical modelling was used to create regulatory networks based on wild‐type RNA and protein expression.Dual activity of AMS was defined by biphasic protein expression in anther tapetal cells, with an initial peak around pollen meiosis and then later during pollen wall development. Direct AMS‐regulated targets exhibit temporal regulation, indicating that additional factors are associated with their regulation.We demonstrate that AMS biphasic expression is essential for pollen development, and defines distinct functional activities during early and late pollen development. Mathematical modelling suggests that AMS may competitively form a protein complex with other tapetum‐expressed transcription factors, and that biphasic regulation is due to repression of upstream regulators and promotion of AMS protein degradation.

Highlights

Anther development is a complex cascade of events regulating the differentiation of specialized cell types within the anther, involving > 1000 stamen-specific transcripts in Arabidopsis (AlvesFerreira et al, 2007)
A number of principal tapetum transcription factors have been identified in Arabidopsis, including DYSFUNCTIONAL TAPETUM1 (DYT1) (Zhang et al, 2006; Feng et al, 2012), ABORTED MICROSPORES (AMS) (Sorensen et al, 2003; Xu et al, 2010, 2014) (both basic helix-loop-helix transcription factors) and MALE STERILITY1 (MS1) (Wilson et al, 2001; Yang et al, 2007a)
We show that AMS function is facilitated by two peaks of protein expression within the tapetum, which are independent of transcriptional control

Summary

Introduction

Anther development is a complex cascade of events regulating the differentiation of specialized cell types within the anther, involving > 1000 stamen-specific transcripts in Arabidopsis (AlvesFerreira et al, 2007). A number of principal tapetum transcription factors have been identified in Arabidopsis, including DYSFUNCTIONAL TAPETUM1 (DYT1) (Zhang et al, 2006; Feng et al, 2012), ABORTED MICROSPORES (AMS) (Sorensen et al, 2003; Xu et al, 2010, 2014) (both basic helix-loop-helix (bHLH) transcription factors) and MALE STERILITY1 (MS1) (a PHD finger-motif transcription factor) (Wilson et al, 2001; Yang et al, 2007a) These are evolutionarily conserved, with orthologues characterized in rice and other cereals (Wilson & Zhang, 2009; Gomez et al, 2015). The dyt mutant causes late meiotic failure during microspore development and prevents correct callose wall formation (Zhang et al., 778 New Phytologist (2017) 213: 778–790 www.newphytologist.com

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Discussion

Conclusion