The involvement of ethylene in programmed cell death and climacteric-like behaviour during the remodelling of lace plant (Aponogeton madagascariensis) leaves

Abstract

Programmed cell death (PCD) plays an important role in several plant developmental processes. The phytohormone ethylene has been implicated in PCD signalling in many plant systems, but it is also important in developmental processes such as seed germination, flowering, and climacteric fruit ripening. Lace plant (Aponogeton madagascariensis (Mirbel) H. Bruggen) is an aquatic monocot that develops perforated leaves via the deletion of cells through developmentally regulated PCD. The plant is ideal for studying PCD; however, little is known about the regulation of cellular death involved in this system. The current study examines ethylene as a potential signalling molecule in lace plant PCD and investigates climacteric-like behaviour during lace plant leaf development. Whole plants were treated with the ethylene biosynthesis inhibitor aminoethoxyvinylglycine (AVG), the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC), or a combination of both. Subsequently, ethylene levels were monitored, and leaf development was analyzed. The results indicate that ethylene is involved in lace plant PCD signalling. AVG-treated plants had significantly lower ethylene outputs and a significant reduction in perforation formation. The inhibitory effect of AVG was recovered when AVG and ACC were applied simultaneously. The data presented here show for the first time, to our knowledge, climacteric-like behaviour during the remodelling of leaves.

Cellular and Molecular Changes Associated with Onion Skin Formation Suggest Involvement of Programmed Cell Death

“…We found that ethylene-response factor (ERF) genes and genes required for JA biosynthesis, such 12-oxophytodienoate reductase (OPR2) gene, and involved in controlling JA responses, such jasmonate ZIM-Domain 1 gene (JAZ1), were overrepresented in the 1st outer scale and may have crucial role in skin formation in the outer scales ( Figure 7 ; Table 2 ). Ethylene is involved in developmental processes that employ PCD such as senescence (Graham et al, 2012), perforation formation in the lace plant (Dauphinee et al, 2012) and in maize endosperm development (Young et al, 1997). …”

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

“…Recent research shows ethylene is involved in regulation of PCD in lace plant during perforation formation and senescence, in a climacteric-like pattern (Dauphinee et al 2012 ). They showed that ethylene production peaks during the window and senescence stages, both in-which PCD is occurring.…”

“…In plants, several genetic components have been associated with PCD: these include receptor-like/Pelle kinases, pattern recognition receptors, stress receptors, reactive oxygen (ROS) sensors, MAPK cascade, hormonal regulators, transcription factors and caspase-like enzymes [reviewed in Rantong and Gunawardena ( 2015 )]. Hormones involved in plant PCD include, but are not limited to salicylic acid (Cao et al 1994 ; Mur et al 2013 ), jasmonic acid (Mur et al 2013 ), and ethylene (Zhao and Schaller 2004 ; Dauphinee et al 2012 ).…”

“…The phytohormone ethylene has been implicated as an important regulator of PCD in plants (Zhao and Schaller 2004 ). Examples of plant PCD that are thought to involve ethylene include, but are not limited to: the hypersensitive response, organ senescence, aerenchyma formation, leaf and petal abscission, endosperm cell death (Young et al 1997 ; reviewed in Bleecker and Kende 2000 ; Trobacher 2009 ; Rogers 2013 ) and perforation formation in the lace plant (Dauphinee et al 2012 ). Ethylene has been shown to promote the onset of senescence (Zacarias and Reid 1990 ; Jing et al 2005 ) and ethylene-insensitive mutants often display delayed senescence (Grbic and Bleecker 1995 ; Oh et al 1997 ; Jing et al 2005 ).…”

“…Despite the lace plant being an excellent model for the study of PCD, little to no molecular work has been carried out on the species and the developmental signalling pathways involved during perforation formation remain unclear. However, lace plant leaves undergoing PCD during perforation formation and senescence emit a significantly high amount of ethylene, while inhibition of ethylene biosynthesis aminoethoxyvinylglycine (AVG) inhibits perforation formation in lace plant leaves (Dauphinee et al 2012 ). An ethylene receptor inhibitor silver nitrate (AgNO 3 ; Gunawardena et al 2006 ) was also shown to result in significant reductions in the number of perforations within leaves.…”