Nitric Oxide, Ethylene, and Auxin Cross Talk Mediates Greening and Plastid Development in Deetiolating Tomato Seedlings

Abstract

The transition from etiolated to green seedlings involves the conversion of etioplasts into mature chloroplasts via a multifaceted, light-driven process comprising multiple, tightly coordinated signaling networks. Here, we demonstrate that light-induced greening and chloroplast differentiation in tomato (Solanum lycopersicum) seedlings are mediated by an intricate cross talk among phytochromes, nitric oxide (NO), ethylene, and auxins. Genetic and pharmacological evidence indicated that either endogenously produced or exogenously applied NO promotes seedling greening by repressing ethylene biosynthesis and inducing auxin accumulation in tomato cotyledons. Analysis performed in hormonal tomato mutants also demonstrated that NO production itself is negatively and positively regulated by ethylene and auxins, respectively. Representing a major biosynthetic source of NO in tomato cotyledons, nitrate reductase was shown to be under strict control of both phytochrome and hormonal signals. A close NO-phytochrome interaction was revealed by the almost complete recovery of the etiolated phenotype of red light-grown seedlings of the tomato phytochrome-deficient aurea mutant upon NO fumigation. In this mutant, NO supplementation induced cotyledon greening, chloroplast differentiation, and hormonal and gene expression alterations similar to those detected in light-exposed wild-type seedlings. NO negatively impacted the transcript accumulation of genes encoding phytochromes, photomorphogenesis-repressor factors, and plastid division proteins, revealing that this free radical can mimic transcriptional changes typically triggered by phytochrome-dependent light perception. Therefore, our data indicate that negative and positive regulatory feedback loops orchestrate ethylene-NO and auxin-NO interactions, respectively, during the conversion of colorless etiolated seedlings into green, photosynthetically competent young plants.

Phytochrome and phytohormone interplay in tomato: impacts on fruit physiology and quality traits

“…Interestingly, Arabidopsis PDV2 has been shown to be transcriptionally regulated by cytokinin signaling, thereby linking the plant hormonal status with the chloroplast division rates in plant cells (Okazaki et al, 2009). Data recently obtained by our research group also indicate that tomato genes encoding key components of the plastid division machinery are strictly regulated by PHY-dependent light perception in deetiolating tomato seedlings (Melo et al, 2016).…”

“…Evidence also indicates that PHY-dependent light perception can influence auxin transport in tomato seedlings, though the mechanisms behind this interaction remain to be elucidated (Liu et al, 2011). With few exceptions (Colón-Carmono et al, 2000;Cluis et al, 2004;Melo et al, 2016), crosstalk events between light and auxin signaling proteins are still poorly described in the literature.…”

“…Cytokinin can mimic the impact of the light stimuli in several photomorphogenic responses, including the etioplast-to-chloroplast conversion and the pigment accumulation in deetiolating seedlings (Chory et al, 1994;Halliday and Fankhauser, 2003;Vandenbussche et al, 2007 (Lin et al, 2009;Wolters and Jürgens, 2009). Among the environmental cues regulating ethylene biosynthesis, PHY-dependent red light perception has received particular attention (de Goeschl et al, 1967;Kang and Burg, 1972;Imaseki et al, 1971;Vandenbussche et al, 2003), indicating a negative influence on ACC levels (Jiao et al, 1987;Melo et al, 2016) as well as on the ACO and ACS transcript levels (Foo et al, 2006). Studies performed in Arabidopsis indicated that AtPIF5 promotes AtACS expression, and the PHYB-mediated targeting of AtPIF5 for proteasomal degradation proteolysis seems to play a major role in the light-dependent repression of AtACS expression (Khanna et al, 2007).…”

“…Activity of ACO was determined according to Bulens et al (2011), with the modifications described in Melo et al (2016).…”

“…The vial was flushed with ethylene-free air (1 L min -1 ) for 5 min and incubated for 60 minutes under specific experimental conditions, as appropriate. After incubation, 1-mL gas samples were analyzed as described in Melo et al (2016).…”