Inositol polyphosphate 5-phosphatase-controlled Ins(1,4,5)P3/Ca2+ is crucial for maintaining pollen dormancy and regulating early germination of pollen

Abstract

SUMMARYAppropriate pollen germination is crucial for plant reproduction. Previous studies have revealed the importance of dehydration in maintaining pollen dormancy; here, we show that phosphatidylinositol pathway-controlled Ins(1,4,5)P 3 /Ca 2+ levels are crucial for maintaining pollen dormancy in Arabidopsis thaliana. An interesting phenotype, precocious pollen germination within anthers, results from a disruption of inositol polyphosphate 5-phosphatase 12 (5PT12). The knockout mutant 5pt12 has normal early pollen development and pollen dehydration, and exhibits hypersensitive ABA responses, indicating that precocious pollen germination is not caused either by abnormal dehydration or by suppressed ABA signaling. Deficiency of 5PT13 (a close paralog of 5PT12) synergistically enhances precocious pollen germination. Both basal Ins(1,4,5)P 3 levels and endogenous Ca 2+ levels are elevated in pollen from 5pt12 mutants, and 5pt12 5pt13 double mutants show an even higher precocious germination rate along with much higher levels of Ins(1,4,5)P 3 /Ca 2+ . Strikingly, exogenous Ca 2+ stimulates the germination of wild-type pollen at floral stage 12, even in very low humidity, both in vitro and in vivo, and treatment with BAPTA, a [Ca 2+ ] cyt inhibitor, reduces the precocious pollen germination rates of 5pt12, 5pt13 and 5pt12 5pt13 mutants. These results indicate that the increase in the levels of Ins(1,4,5)P 3 /Ca 2+ caused by deficiency of inositol polyphosphate 5-phosphatases is sufficient to break pollen dormancy and to trigger early germination. The study reveals that independent of dehydration, the control of Ins(1,4,5)P 3 /Ca 2+ levels by Inositol polyphosphate 5-phosphatases is crucial for maintaining pollen dormancy.

Phosphoinositide signaling in plant development

“…In recent years, PIs have emerged as central regulators of plant function and development, and a number of important and severe plant phenotypes have been reported when plant PI metabolism is perturbed Nelson, 2009, 2004;Chen et al, 2008;Ercetin et al, 2008;Golani et al, 2013;Gunesekera et al, 2007;Ischebeck et al, 2008Ischebeck et al, , 2011Ischebeck et al, , 2013Kaye et al, 2011;Kusano et al, 2008;Löfke et al, 2008;Mei et al, 2012;Novakova et al, 2014;Parker et al, 2000;Preuss et al, 2006;Rodriguez-Villalon et al, 2015;Sousa et al, 2008;Stenzel et al, 2008;Tejos et al, 2014;Wang et al, 2012;Williams et al, 2005;Zhong et al, , 2005. The perturbation of PI signaling components in Arabidopsis, for example, gives rise to a variety of phenotypes affecting multiple tissue types and aspects of plant development (summarized in Table 1).…”

Plant phosphoinositide-dependent phospholipases C: Variations around a canonical theme

“…Studies of the supo1 mutant of Arabidopsis defective in inositol polyphosphate 1-phosphatase have shown that regulation of auxin distribution through PIN transporters is mediated by cytosolic calcium release controlled by IP3 [182]. It was also shown that elevated IP3 levels in Arabidopsis inositol polyphosphate 5-phosphatase mutants resulted in elevated concentrations and altered distributions of cytosolic Ca 2+ in developing pollen [183]. However, there is no direct genetic or molecular evidence for the existence of plant IP3 receptors.…”

Arabidopsis Histone Methylase CAU1/PRMT5/SKB1 Acts as an Epigenetic Suppressor of the Calcium Signaling Gene CAS to Mediate Stomatal Closure in Response to Extracellular Calcium

“…Calcium levels were calculated and pseudocolored according to the color scale as described (Wang et al, 2012b). Briefly, pseudocolor ratio images of calcium level were calculated with the Olympus Fluoview ver.…”