Disruption of Arabidopsis neutral ceramidases 1 and 2 results in specific sphingolipid imbalances triggering different phytohormone‐dependent plant cell death programmes

Abstract

Summary Sphingolipids act as regulators of programmed cell death (PCD) and the plant defence response. The homeostasis between long‐chain base (LCB) and ceramide (Cer) seems to play an important role in executions of PCD. Therefore, deciphering the role of neutral ceramidases (NCER) is crucial to identify the sphingolipid compounds that trigger and execute PCD. We performed comprehensive sphingolipid and phytohormone analyses of Arabidopsis ncer mutants, combined with gene expression profiling and microscopic analyses. While ncer1 exhibited early leaf senescence (developmentally controlled PCD – dPCD) and an increase in hydroxyceramides, ncer2 showed spontaneous cell death (pathogen‐triggered PCD‐like – pPCD) accompanied by an increase in LCB t18:0 at 35 d, respectively. Loss of NCER1 function resulted in accumulation of jasmonoyl‐isoleucine (JA‐Ile) in the leaves, whereas disruption of NCER2 was accompanied by higher levels of salicylic acid (SA) and increased sensitivity to Fumonisin B1 (FB1). All mutants were also found to activate plant defence pathways. These data strongly suggest that NCER1 hydrolyses ceramides whereas NCER2 functions as a ceramide synthase. Our results reveal an important role of NCER in the regulation of both dPCD and pPCD via a tight connection between the phytohormone and sphingolipid levels in these two processes.

Phloem Exudate Protein Profiles during Drought and Recovery Reveal Abiotic Stress Responses in Tomato Vasculature

“…While few studies exploring hydroxyceramide accumulation in plants exist, many reports show a link between hydroxyceramide levels and cell signaling, membrane homeostasis, and cell death in mammals [ 75 ]. However, it was recently shown that an Arabidopsis Atncer1 knockout resulted in elevated hydroxyceramide levels, accumulation of jasmonoyl-isoleucine in leaves, and resulted in early leaf senescence [ 76 ]. Our findings suggest that ceramide metabolism in the phloem might prepare plants for leaf loss as a proactive mechanism for severe drought.…”

Fumonisin B1: A Tool for Exploring the Multiple Functions of Sphingolipids in Plants

“…ACER1-silenced plants and acer1 mutant plants were sensitive to FB1, and ACER1overexpressing plants were relatively resistant to FB1 (Wu et al, 2015a). Disrupting neutral ceramidase 2 (NCER2), which likely functions as a ceramide synthase, increased sensitivity to FB1 in Arabidopsis (Zienkiewicz et al, 2019). Bax Inhibitor-1 (BI-1), an evolutionarily conserved cell death suppressor in mammals and plants (Kawai-Yamada et al, 2001;Mosblech et al, 2009;Christensen and Kolomiets, 2011), attenuates cell death progression triggered by FB1 in plants (Watanabe and Lam, 2006).…”

Sphingolipids in plants: a guidebook on their function in membrane architecture, cellular processes, and environmental or developmental responses

“…During PCD, the modulation of the ratio between LCB and ceramide quantity impacts jasmonate‐ and SA‐signaling pathways (Fig. 4) [83,84]. To summarize, phytohormones can induce SLs‐mediated signaling, like in the case of ABA and S1P, but SLs can also feedback on hormone‐signaling as for the LCB/ceramide ratio and jasmonate‐ and SA‐signaling.…”