PERSISTENT TAPETAL CELL2 Is Required for Normal Tapetal Programmed Cell Death and Pollen Wall Patterning

Abstract

The timely programmed cell death (PCD) of the tapetum, the innermost somatic anther cell layer in flowering plants, is critical for pollen development, including the deposition and patterning of the pollen wall. Although several genes involved in tapetal PCD and pollen wall development have been characterized, the underlying regulatory mechanism remains elusive. Here we report that PERSISTENT TAPETAL CELL2 (PTC2), which encodes an AT-hook nuclear localized protein in rice (Oryza sativa), is required for normal tapetal PCD and pollen wall development. The mutant ptc2 showed persistent tapetal cells and abnormal pollen wall patterning including absent nexine, collapsed bacula, and disordered tectum. The defective tapetal PCD phenotype of ptc2 was similar to that of a PCD delayed mutant, ptc1, in rice, while the abnormal pollen wall patterning resembled that of a pollen wall defective mutant, Transposable Element Silencing Via AT-Hook, in Arabidopsis (Arabidopsis thaliana). Levels of anther cutin monomers in ptc2 anthers were significantly reduced, as was expression of a series of lipid biosynthetic genes. PTC2 transcript and protein were shown to be present in the anther after meiosis, consistent with the observed phenotype. Based on these data, we propose a model explaining how PTC2 affects anther and pollen development. The characterization of PTC2 in tapetal PCD and pollen wall patterning expands our understanding of the regulatory network of male reproductive development in rice and will aid future breeding approaches.

Abnormal Anther Development Leads to Lower Spikelet Fertility in Rice (Oryza Sativa L.) Under High Temperature During the Panicle Initiation Stage

“…3V). Similarly, Uzair et al [34] found marginal differences in the patterning of nano-ridges on the outer surface, as well as in the distribution of Ubisch bodies, on the inner surface of anthers in rice ptc2 mutants, which resulted in decreased pollen viability in comparison with that of wild-type plants. However, in SY63 plants, HT had no substantial effect on Ubisch bodies or anther cuticles (Fig.…”

“…The tapetum, the innermost layer in the anther wall, serves as an active nutrient source for neighboring microspores [34,39], and abnormal tapetum degeneration results in pollen sterility in photoperiod and thermosensitive genic male-sterile rice [40,41] and rice mutants [34]. These previous reports indicate that termination of secretory-type tapetum development and disruption of tapetal functions is partly responsible for pollen viability.…”

“…These results show that HT disrupted tapetum degradation in LYPJ. Similarly, halted and incomplete tapetum degradation was reported in rice ptc2 mutants [34] and rice plants under chilling [37], and as well in tomato and cotton plants under heat stress [25,38]. Regarding causes for abnormal tapetum degradation, Mamun et al [37] revealed that vacuolation and hypertrophy of the tapetum under chilling was caused by osmotic imbalance, which was triggered by the reabsorption of callose breakdown products in the absence of OsMST8 activity.…”

OsMS188 Is a Key Regulator of Tapetum Development and Sporopollenin Synthesis in Rice

“…We speculate that TDR regulates pollen wall formation by activating the expression of OsMS188 during anther development. Additionally, GAMYB and PTC2 have also been reported to regulate exine formation and PCD of tapetal cells in rice anther development (Aya et al 2009;Uzair et al 2020). PTC2 is the homologue of TEK, an AT-hook motif nuclear-localized protein essential for nexine formation in Arabidopsis.…”

Oxygen, secreted proteins and small RNAs: mobile elements that govern anther development

“…Key players and developmental programs for early anther development have been extensively studied and described (reviewed in : Timofejeva et al 2013;Kelliher et al 2014;Walbot and Egger 2016; van der Linde and Walbot 2019) (Table 1). Other studies gave insight into late anther and pollen development (for example, see: Dickinson and Bell 1976;Schreiber et al 2004), and by now also provide a sound understanding about involved transcription factors and components for the tapetal cell death and pollen wall formation (for example, Huo et al 2020;Xiong et al 2020;Uzair et al 2020;Lu et al 2020). A recurring Communicated by Dolf Weijers.…”