Evidence of Programmed Cell Death in Post-Phloem Transport Cells of the Maternal Pedicel Tissue in Developing Caryopsis of Maize

Abstract

We present cellular-and ultracellular-level studies here to show developmental programmed cell death (PCD) of placentochalazal (P-C) cell layers in maternal pedicel tissue in developing caryopses of normal seed (Mn1) and in the invertasedeficient miniature (mn1) seed mutant in maize (Zea mays). PCD was evidenced by loss of nuclei and all subcellular membranous organizations in many P-C layers. The terminal deoxynucleotidyl transferase-mediated X-dUTP nick-end labeling (TUNEL) stain that is diagnostic of apoptotic-like PCD identified spatially and temporally two distinctive subdomains, which coincided with nucellar and integumental P-C layers based on their developmental origins. The early phase of PCD in the nucellar P-C was TUNEL negative and was specific to only the fertilized caryopses, indicating that the signaling for PCD in these maternal cells originated in the zygotic tissues. In fact, the initiation of PCD coincided with endosperm cellularization and was rapidly and coordinately completed prior to the beginning of the major storage phase in endosperm. Cell shape in these cell layers was also influenced by the genotype of filial endosperm. The later phase of PCD was restricted to the integumental P-C layers underneath the nucellar cells and was TUNEL positive in both genotypes. The two subdomains of the P-C layers were also distinguishable by unique cell wall-associated phenolic compounds. Based on collective evidence, we infer that the nucellar PCD may have osmolytic etiology and may lead to activation of the post-phloem transport function of the P-C layer, whereas the integumental PCD was senescent related, in particular, protecting the maturing seed against microbes that may be transported from the maternal tissue.Pedicel, a maternal tissue at the base of developing seeds of all higher plants, provides the major structural bridge in the transfer of photoassimilates and nutrients from the mother plant to the filial generation, endosperm, and embryo. In maize (Zea mays), directly underneath the basal endosperm cells and just above the phloem termini in pedicel, is a mat of cells that constitute the placento-chalazal (P-C) layer (Fig. 1B), which is believed to play a critical role in post-phloem transport of water, sugars, and nutrients for developing seeds (Kiesselbach, 1949; Felker and Shannon, 1980;Schel et al., 1984). Although described in various plant species, a P-C region is known to exhibit a high level of anatomical variability in its structural adaptations (for review, see Thorne, 1985). P-C layers are perhaps best developed in tropical crops such as maize and sorghum (Sorghum bicolor), which show assimilate transport from only the base of the caryopsis. In fact, the functional importance of a normal P-C layer is best exemplified in the miniature 1 (mn1) seed mutation in maize that shows greatly reduced size of the endosperm due to a premature withdrawal of the P-C layer from developing seed, causing a physical discontinuity, a gap, between the source and sink tissues (Lowe and Nelson, 1946). T...

Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

“…Related to our finding, the loss-of-function of CWIN in the maize mutant mn1 led to a reduction of cell division and expansion in the mutant endosperm (Vilhar et al, 2002) and induction of PCD in the placentochalazal region of kernels (Kladnik et al, 2004). In our case, however, LMHS increased tomato fruit abortion in the wild type through triggering PCD (Figs.…”

Variability of breeding system, caryopsis microstructure and germination in annual and perennial species of the genus Brachypodium P. Beauv.

“…5B) and its pigment strand is highly saturated by suberin and phenolics. This differentiation of the testa layers supports Kladnik et al's data (Kladnik et al 2004). Probably, the most important factor for quick germination is the structure of caryopsis attachment to the lemma-palea base.…”

“…Probably, the most important factor for quick germination is the structure of caryopsis attachment to the lemma-palea base. Kladnik et al (2004) found the different phenolics in a maize grain attachment structure. This area is free from suberin-phenolics in all ecotypes of annual B. distachyon (Fig.…”

Cytokinins and Their Possible Role in Seed Size and Seed Mass Determination in Maize

“…4a). The peak of CK concentration before 12 DAP has been previously suggested to be associated with the induction of programmed cell death in the placento-chalazal region of the caryopsis pedicel (Rijavec et al, 2011), as its essential developmental phase (Kladnik et al, 2004). The proper activity of the placento-chalazal region is crucial for the transport of photosynthates from the maternal to the filial tissues of the caryopsis.…”