The maize transfer cell‐specific type‐A response regulator ZmTCRR‐1 appears to be involved in intercellular signalling

Abstract

SummaryResponse regulators are signal-transduction molecules present in bacteria, yeast and plants, acting as relays for environmental challenges. This paper reports the characterization of a Zea mays gene, ZmTCRR-1, that codes for a member of the type-A response regulator class of proteins. The gene was found to be expressed exclusively in the endosperm transfer-cell layer 8-14 days after pollination, when transfer-cell differentiation is most active. The promoter of ZmTCRR-1 was strongly transactivated in heterologous systems by the transfer cell-specific transcription factor ZmMRP-1. The ZmTCRR-1 protein was detected not only in the transfer-cell layer, but also in the conductive tissue deep inside the endosperm, where there is no transcription of the gene. This suggests that two-component systems might be involved in intercellular signal transmission, in contrast to the generally held belief that these systems are involved only in cell-autonomous pathways.

RNA Sequencing of Laser-Capture Microdissected Compartments of the Maize Kernel Identifies Regulatory Modules Associated with Endosperm Cell Differentiation

“…Furthermore, the BETLspecific TF gene MRP-1, previously shown to be involved in regulation of BETL differentiation (Gómez et al, 2002(Gómez et al, , 2009, was also detected in M18 with a high MM score (1.00; Supplemental Data Set 4). This is consistent with its role as an activator of many BETLspecific genes, including BETL-1, BETL-9, BETL-10, BAP-2, MEG-1, TCRR-1, and TCRR-2 (Gómez et al, 2002(Gómez et al, , 2009Gutiérrez-Marcos et al, 2004;Muñiz et al, 2006Muñiz et al, , 2010. Therefore, these data suggest that MRP-1 acts as a major regulator of a subset of genes in the M18 coexpression module.…”

“…These genes showed CS scores in the given compartments ranging from 0.47 to 0.99. Third, we summarized previously reported in situ hybridization or promoter activity data for cell-specific genes from the literature (Hueros et al, 1995(Hueros et al, , 1999Magnard et al, 2000Magnard et al, , 2003Serna et al, 2001;Woo et al, 2001;Gómez et al, 2002Gómez et al, , 2009Gutiérrez-Marcos et al, 2004;Wisniewski and Rogowsky, 2004;Balandín et al, 2005;Massonneau et al, 2005;Muñiz et al, 2006Muñiz et al, , 2010Royo et al, 2014) and also found these genes to have a relatively high range of CS scores (0.51 to 0.99). Altogether, these comprise 44 genes showing cell-specific expression in the endosperm (Supplemental Table 6).…”

“…The BETL transports nutrients from the maternal tissue into the endosperm and is important for the proper development of the endosperm and the endosperm's capacity as a storage organ Costa et al, 2012). Based on the available data (Baranowskij et al, 1994;Gómez et al, 2002Gómez et al, , 2009Gutiérrez-Marcos et al, 2004;Barrero et al, 2006;Muñiz et al, 2006Muñiz et al, , 2010 including our identification of the coexpression module M18 and its association with GATA-rich sequence motifs (discussed above), we hypothesized that a GRN for BETL differentiation is minimally composed of MRP-1 and a large set of target genes that are activated upon binding of MRP-1 to Motifs 3, 6, and 8. A close examination of all the submotifs of the 10 motifs enriched for M18 showed that each of the motifs is represented by two to 21 submotifs that appeared one to 90 times within the promoters of the M18 genes (Supplemental Table 10).…”

“…The M18 module contained nearly all of the previously identified BETL-expressed genes (Hueros et al, 1995(Hueros et al, , 1999Cheng et al, 1996;Doan et al, 1996;Serna et al, 2001;Magnard et al, 2003;Gutiérrez-Marcos et al, 2004;Massonneau et al, 2005;Gruis et al, 2006;Muñiz et al, 2006Muñiz et al, , 2010Brugière et al, 2008;Gómez et al, 2009), including BETL-1, 3, 4, 9, and 10; BAP-1A, 1B, 2, 3A, and 3B; TCRR-1 and 2; and INCW2 (CELL WALL INVERTASE2), EBE-2 (EMBRYO SAC/BASAL ENDOSPERM-LAYER/EMBRYO-SURROUNDING REGION-2), IPT-2 (ISOPENTENYL TRANS-FERASE-2), and CC-8 (CORN CYSTATIN-8) (Supplemental Data Set 4). In addition, this module contained 11 of the 13 MEG genes (with MEG-4 and MEG-14 being the two exceptions) that have been identified in the B73 genome (Supplemental Data Set 4), including MEG-1, which is a BETL-specific gene that has been shown to be important for the development and differentiation of the BETL (Costa et al, 2012).…”

ZmPIN1-Mediated Auxin Transport Is Related to Cellular Differentiation during Maize Embryogenesis and Endosperm Development

“…The aleurone is an epidermal layer that covers the endosperm, secretes hydrolytic enzymes, and mobilizes storage reserves from the starchy endosperm during seed germination (Becraft, 2001;Olsen, 2001). The basal endosperm transfer layer (BETL) is a highly specialized tissue with deep cell ingrowths at the basal surface that facilitate nutrient uptake from the apoplastic space in the placentochalazal region (Thompson et al, 2001) and is characterized by the BETL class of genes (Hueros et al, 1995;Muniz et al, 2006). Among the BETL genes, ZmTCI-1, a Myb-related transcription factor, has been shown to be a key regulator of transfer cell differentiation and function (Barrero et al, 2009).…”