AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen

Abstract

Sexual plant reproduction depends on the production and differentiation of functional gametes by the haploid gametophyte generation. Currently, we have a limited understanding of the regulatory mechanisms that have evolved to specify the gametophytic developmental programs. To unravel such mechanisms, it is necessary to identify transcription factors (TF) that are part of such haploid regulatory networks. Here we focus on bZIP TFs that have critical roles in plants, animals and other kingdoms. We report the functional characterization of Arabidopsis thaliana AtbZIP34 that is expressed in both gametophytic and surrounding sporophytic tissues during flower development. T-DNA insertion mutants in AtbZIP34 show pollen morphological defects that result in reduced pollen germination efficiency and slower pollen tube growth both in vitro and in vivo. Light and fluorescence microscopy revealed misshapen and misplaced nuclei with large lipid inclusions in the cytoplasm of atbzip34 pollen. Scanning and transmission electron microscopy revealed defects in exine shape and micropatterning and a reduced endomembrane system. Several lines of evidence, including the AtbZIP34 expression pattern and the phenotypic defects observed, suggest a complex role in male reproductive development that involves a sporophytic role in exine patterning, and a sporophytic and/or gametophytic mode of action of AtbZIP34 in several metabolic pathways, namely regulation of lipid metabolism and/or cellular transport.

Wide-scale screening of T-DNA lines for transcription factor genes affecting male gametophyte development in Arabidopsis

“…However, the roles of transcription factors in complex networks should be regarded as different regulators and can trigger various biochemical processes that ultimately affect similar cellular processes and functions, such as cytoskeleton organization, cell cycling, cellular transport, cell wall metabolism, etc. Sex Plant Reprod (2012) 25:39-60 43 Such pleiotropic activity has repeatedly been reported (Gibalová et al 2009;Twell et al 2006;Verelst et al 2007). Five complex developmental and functional disorder classes were observed in comparison with standard wild-type phenotype.…”

“…2c). Despite their unknown composition, they were likely formed as a consequence of impaired metabolical and/or secretory pathways, as recently published for bZIP family transcription factor AtbZIP34 (Gibalová et al 2009). The most serious and complex phenotypic defect(s) led to complete cell abortion (Fig.…”

“…In rice, OsbZIP72 (group A bZIP) is a positive regulator of ABA response and drought tolerance (Lu et al 2009). Recently, group E bZIP TF AtbZIP34 (At2g42380) was demonstrated to fulfill multiple roles in pollen development; it controls cellular transport, lipid metabolism, and cell wall patterning (Gibalová et al 2009). Our observations confirmed the published results by analyses of two T-DNA insertion lines: SALK_018864 (At2g42380) plants produced 25-30% pollen with cytoplasmic inclusions, 25-30% small pollen grains, 15% aborted pollen, 10% two-celled pollen, and SALK_128336 line (At2g42380) showed 20-25% linear MGU and 5% of two-celled pollen ( Table 2).…”

“…HAPLESS5 (HAP5) encodes AP2-domain protein, and its mutation causes pollen morphological defects and abortion ). Finally, AtbZIP34 controls pollen wall patterning and affects several metabolic pathways (Gibalová et al 2009). The interaction map of MADS-box genes (de Folter et al 2005;Veron et al 2007) and particularly the male gametophyte-specific regulatory network of their AtMIKC* subgroup (Verelst et al 2007) belong among the best characterized.…”

Combined Large-Scale Phenotyping and Transcriptomics in Maize Reveals a Robust Growth Regulatory Network

“…These cell wallrelated genes as well as other genes of subnetwork 2 were coexpressed with GRMZM2G045534, an ATP-citrate lyase whose down-regulation of Arabidopsis orthologs results in pleiotropic phenotypes, including reduced size (Fatland et al, 2005). Also, three TFs were highly coexpressed with the genes in subnetwork 2: GATA TF (GRMZM2G101058) described above, a bZIP TF (GRMZM2G052102) of which the Arabidopsis orthologous mutant shows cell wall defects in pollen (Gibalová et al, 2009), and a TRIHELIX TF (GRMZM2G314660). The latter shows homology to Arabidopsis GTL1, a master regulator that negatively regulates cell growth (Breuer et al, 2012).…”