Lace plant ethylene receptors, AmERS1a and AmERS1c, regulate ethylene-induced programmed cell death during leaf morphogenesis

Abstract

The lace plant, Aponogeton madagascariensis, is an aquatic monocot that forms perforations in its leaves as part of normal leaf development. Perforation formation occurs through developmentally regulated programmed cell death (PCD). The molecular basis of PCD regulation in the lace plant is unknown, however ethylene has been shown to play a significant role. In this study, we examined the role of ethylene receptors during perforation formation. We isolated three lace plant ethylene receptors AmERS1a, AmERS1b and AmERS1c. Using quantitative PCR, we examined their transcript levels at seven stages of leaf development. Through laser-capture microscopy, transcript levels were also determined in cells undergoing PCD and cells not undergoing PCD (NPCD cells). AmERS1a transcript levels were significantly lower in window stage leaves (in which perforation formation and PCD are occurring) as compared to all other leaf developmental stages. AmERS1a and AmERS1c (the most abundant among the three receptors) had the highest transcript levels in mature stage leaves, where PCD is not occurring. Their transcript levels decreased significantly during senescence-associated PCD. AmERS1c had significantly higher transcript levels in NPCD compared to PCD cells. Despite being significantly low in window stage leaves, AmERS1a transcripts were not differentially expressed between PCD and NPCD cells. The results suggested that ethylene receptors negatively regulate ethylene-controlled PCD in the lace plant. A combination of ethylene and receptor levels determines cell fate during perforation formation and leaf senescence. A new model for ethylene emission and receptor expression during lace plant perforation formation and senescence is proposed.

Gene Mapping, Genome-Wide Transcriptome Analysis, and WGCNA Reveals the Molecular Mechanism for Triggering Programmed Cell Death in Rice Mutant pir1

“…Many different signal molecules, such as plant hormones including jasmonic acid (JA), brassinosteroid (BR), salicylic acid (SA), and ethylene (ET), are closely related to the PCD process [ 32 , 33 , 34 , 35 ]. Lipoxygenase (LOX) is an essential enzyme for JA synthesis, and activation of LOX expression can significantly induce the synthesis and accumulation of JA [ 36 , 37 ].…”

Remodelling of lace plant leaves: antioxidants and ROS are key regulators of programmed cell death

“…Candidates include phytohormones such as ethylene, salicylic acid, and jasmonates, or even ROS themselves. Ethylene has been implicated in lace plant PCD signaling during perforation formation and senescence (Dauphinee et al 2012 ; Rantong et al 2015 ); however, the relationship between ethylene, antioxidants, and ROS remains unknown. Positive feedback loops are known to exist between various hormones, reactive nitrogen species, and ROS, which ultimately trigger downstream effectors such as nucleases and proteases that carry out PCD (Van Breusegem and Dat 2006 ).…”

CsAP3: A Cucumber Homolog to Arabidopsis APETALA3 with Novel Characteristics

“…The plant would need to sense the internal and external environment sensitively and flexibly and maintain a beneficial balance of male and female ratio of flowers within a single plant. In fact, the connection of a minor decrease in expression of the ethylene receptor with critical developmental events exists not only in cucumber as ethylene-induced stamen-specific DNA damage, but also in the Aponogeton madagascariensis (lace plant), where it results in perforations in leaves through programmed cell death ( Rantong et al, 2015 ). These phenomena highlight that in some situations, moderate regulation of gene expression may play important roles in biological processes.…”