INDUCER OF CBF EXPRESSION 1 is a male fertility regulator impacting anther dehydration in Arabidopsis

Abstract

INDUCER OF CBF EXPRESSION 1 (ICE1) encodes a MYC-like basic helix-loop-helix (bHLH) transcription factor playing a critical role in plant responses to chilling and freezing stresses and leaf stomata development. However, no information connecting ICE1 and reproductive development has been reported. In this study, we show that ICE1 controls plant male fertility via impacting anther dehydration. The loss-of-function mutation in ICE1 gene in Arabidopsis caused anther indehiscence and decreased pollen viability as well as germination rate. Further analysis revealed that the anthers in the mutant of ICE1 (ice1-2) had the structure of stomium, though the epidermis did not shrink to dehisce. The anther indehiscence and influenced pollen viability as well as germination in ice1-2 were due to abnormal anther dehydration, for most of anthers dehisced with drought treatment and pollen grains from those dehydrated anthers had similar viability and germination rates compared with wild type. Accordingly, the sterility of ice1-2 could be rescued by ambient dehydration treatments. Likewise, the stomatal differentiation of ice1-2 anther epidermis was disrupted in a different manner compared with that in leaves. ICE1 specifically bound to MYC-recognition elements in the promoter of FAMA, a key regulator of guard cell differentiation, to activate FAMA expression. Transcriptome profiling in the anther tissues further exhibited ICE1-modulated genes associated with water transport and ion exchange in the anther. Together, this work reveals the key role of ICE1 in male fertility control and establishes a regulatory network mediated by ICE1 for stomata development and water movement in the anther.

miR167 limits anther growth to potentiate anther dehiscence

“…mir167a and mARF8 pollen had slightly decreased viability and in vitro germination rate, similarly to pollen from inadequately desiccated ice1 mutant anthers (Wei et al, 2018). Delayed desiccation of the anther and its pollen might also delay pollen maturation, or alternatively allow pollen to bypass desiccation and dormancy, as suggested by the occasional pollen germination we observed in mARF8 anthers.…”

“…Prolonged hydration might also delay cell wall breakdown in the septum and/or stomium through regulatory pathways regulated by cytoplasmic or apoplastic water potential. Other factors needed for dehiscence such as stomatal differentiation or lignification (Yang et al, 2007;Wei et al, 2018) were apparently unaffected in miR167 pathway mutants. Changes in growth rate are also important for developmental events such as sperm release from pollen, where peptide signals from the female gametophyte induce growth imbalance leading to pollen tube rupture and sperm release (Ge et al, 2017).…”

“…The delay in desiccation in miR167 pathway mutants might limit production of mechanical forces to crack open the stomium and/or to evert the locule walls to release pollen (Wilson et al, 2011;Nelson et al, 2012;Wei et al, 2018). In this scenario, enlarged mutant anthers could preclude or delay generation of sufficient mechanical force, either because of delayed shrinkage to an appropriate size, or if greater forces are needed to evert the enlarged mutant locule walls than are needed in wild-type anthers.…”

The plant stomatal lineage at a glance

“…For instance, following up on these data (Adrian et al, 2015) led to identification of the stomatal lineage-specific CYCLIN D7;1 (CYCD7;1), which is part of a system that ensures GMCs divide onceand only onceto produce a pair of GCs (Weimer et al, 2018; and further elaborated in Han et al, 2018). A role for ICE1 in anther dehydration regulation was revealed by over-representation of GC-expressed genes among ICE1-regulated genes in anthers (Wei et al, 2018). GC cell walls are unique among Arabidopsis cells with regards to the composition and modification of cell wall matrix polymers; the stomatal lineage transcriptional map was noted as a valuable resource for identification of GC-specific cell wall-modifying enzymes (Rui et al, 2018).…”

BrrICE1.1 is associated with putrescine synthesis through regulation of the arginine decarboxylase gene in freezing tolerance of turnip (Brassica rapa var. rapa)

“…However, it was not clear which polyamine pathway gene acts on PtrICE1 to regulate polyamine level [24]. In the process of plants responding to cold, ICE1 plays a critical role in response to environmental changes by positively regulating genes through binding speci cally to the MYC element in the promoter region which is considered as a classical mode of action on ICE1 [20,36]. Our results of BrrADC2.2 and BrrICE1.1 transgenic and RNAi roots showed that the increase of putrescine content by overexpression of BrrICE1.1 was mainly due to the binding of BrrICE1.1 to the MYC element of BrrADC2.2 promoter region in turnip (Fig.…”