A Combinatorial Interplay Among the 1-Aminocyclopropane-1-Carboxylate Isoforms Regulates Ethylene Biosynthesis inArabidopsis thaliana

Abstract

Ethylene (C 2 H 4 ) is a unique plant-signaling molecule that regulates numerous developmental processes. The key enzyme in the two-step biosynthetic pathway of ethylene is 1-aminocyclopropane-1-carboxylate synthase (ACS), which catalyzes the conversion of S-adenosylmethionine (AdoMet) to ACC, the precursor of ethylene. To understand the function of this important enzyme, we analyzed the entire family of nine ACS isoforms (ACS1, ACS2, ACS4-9, and ACS11) encoded in the Arabidopsis genome. Our analysis reveals that members of this protein family share an essential function, because individual ACS genes are not essential for Arabidopsis viability, whereas elimination of the entire gene family results in embryonic lethality. Phenotypic characterization of single and multiple mutants unmasks unique but overlapping functions of the various ACS members in plant developmental events, including multiple growth characteristics, flowering time, response to gravity, disease resistance, and ethylene production. Ethylene acts as a repressor of flowering by regulating the transcription of the FLOWERING LOCUS C. Each single and high order mutant has a characteristic molecular phenotype with unique and overlapping gene expression patterns. The expression of several genes involved in light perception and signaling is altered in the high order mutants. These results, together with the in planta ACS interaction map, suggest that ethylene-mediated processes are orchestrated by a combinatorial interplay among ACS isoforms that determines the relative ratio of homo-and heterodimers (active or inactive) in a spatial and temporal manner. These subunit isoforms comprise a combinatorial code that is a central regulator of ethylene production during plant development. The lethality of the null ACS mutant contrasts with the viability of null mutations in key components of the ethylene signaling apparatus, strongly supporting the view that ACC, the precursor of ethylene, is a primary regulator of plant growth and development.

Ethylene Exerts Species-Specific and Age-Dependent Control of Photosynthesis

“…Eventually, ethylene-insensitive mutants 233 age and show senescence, suggesting that ethylene controls both the rate and timing of leaf 234 senescence (Grbic & Bleecker, 1995). Delayed senescence and concomitant decline in chlorophyll 235 content and photosynthesis has also been observed in antisense plants for ACO of tomato (Picton et 236 al., 1993;John et al, 1995;Jensen & Veierskov, 1998) and acs6 mutants of the C4 plant maize 237 (Young et al, 2004), but not for acs mutants of Arabidopsis (Tsuchisaka et al, 2009 (Lanahan et al, 1994). In general, we conclude that a temporal 243 exposure to ethylene stimulates leaf senescence in mature leaves, while continuous exposure 244 instead causes altered leaf development.…”

Genome-Wide Association Mapping and Genomic Prediction Elucidate the Genetic Architecture of Morphological Traits in Arabidopsis

“…Otherwise, plants growing at higher latitudes might have adapted to cooler climates and therefore show a lower activation point for heat-induced petiole elongation (Koini et al, 2009;van Zanten et al, 2009). It is worthwhile to note here that mutations in the ACS gene family also affect FLC expression and FT (Tsuchisaka et al, 2009). Some mutations tend to induce flowering while others, concomitant with a decrease in ethylene production, seem to delay flowering.…”

“…The low significance might be due to redundancy and/or the Col-0 genetic background. Indeed, the PL and the PL/LL in an acs octuple mutant and in an ethylene insensitive mutant, ein2-1 (Alonso et al, 1999;Tsuchisaka et al, 2009), were significantly reduced, although concomitant with a reduction in LL (Fig. 3I).…”

“…ACS enzymes, forming homo-and heterodimers, are thought to catalyze the rate-limiting step in ethylene biosynthesis converting S-adenosyl-LMet into 1-aminocyclopropane-1-carboxylate, the precursor of ethylene (Bleecker and Kende, 2000). Analyses of single, double, and multiple acs mutants revealed that ACS enzymes play essential roles in leaf development, FT, disease resistance, and ethylene production (Tsuchisaka et al, 2009). …”

Azolla, a little fern with massive green potential

“…6). Paralogues of ACC synthase in seed plants are differentially regulated in response to varying developmental or environmental stimuli 19 . Thus, it is plausible that the expansion of the ACC synthase family was coupled with the origin of ACC oxidase in seed plants to create a regulated ethylene biosynthetic pathway.…”