Ethylene Biosynthesis Is Promoted by Very-Long-Chain Fatty Acids during Lysigenous Aerenchyma Formation in Rice Roots

Abstract

In rice (Oryza sativa) roots, lysigenous aerenchyma, which is created by programmed cell death and lysis of cortical cells, is constitutively formed under aerobic conditions, and its formation is further induced under oxygen-deficient conditions. Ethylene is involved in the induction of aerenchyma formation. reduced culm number1 (rcn1) is a rice mutant in which the gene encoding the ATP-binding cassette transporter RCN1/OsABCG5 is defective. Here, we report that the induction of aerenchyma formation was reduced in roots of rcn1 grown in stagnant deoxygenated nutrient solution (i.e. under stagnant conditions, which mimic oxygen-deficient conditions in waterlogged soils). 1-Aminocyclopropane-1-carboxylic acid synthase (ACS) is a key enzyme in ethylene biosynthesis. Stagnant conditions hardly induced the expression of ACS1 in rcn1 roots, resulting in low ethylene production in the roots. Accumulation of saturated very-long-chain fatty acids (VLCFAs) of 24, 26, and 28 carbons was reduced in rcn1 roots. Exogenously supplied VLCFA (26 carbons) increased the expression level of ACS1 and induced aerenchyma formation in rcn1 roots. Moreover, in rice lines in which the gene encoding a fatty acid elongase, CUT1-LIKE (CUT1L; a homolog of the gene encoding Arabidopsis CUT1, which is required for cuticular wax production), was silenced, both ACS1 expression and aerenchyma formation were reduced. Interestingly, the expression of ACS1, CUT1L, and RCN1/OsABCG5 was induced predominantly in the outer part of roots under stagnant conditions. These results suggest that, in rice under oxygen-deficient conditions, VLCFAs increase ethylene production by promoting 1-aminocyclopropane-1-carboxylic acid biosynthesis in the outer part of roots, which, in turn, induces aerenchyma formation in the root cortex.Aerenchyma formation is a morphological adaptation of plants to complete submergence and waterlogging of the soil, and facilitates internal gas diffusion (Armstrong,

Regulation of Root Traits for Internal Aeration and Tolerance to Soil Waterlogging-Flooding Stress

“…Interestingly, the death of root cortical cells (sometimes called root cortical senescence) is enhanced in maize and barley under drought or Figure 2. Model of the signaling processes for inducible aerenchyma formation in rice roots, based mainly on recent findings by Yamauchi et al (2015Yamauchi et al ( , 2017aYamauchi et al ( , 2017b. Under waterlogged (or stagnant) conditions, the entry (diffusion) of oxygen from the atmosphere into soil is impeded by restricted gas exchange, which results in low oxygen levels, whereas ethylene levels in roots are elevated due to the restricted gas exchange.…”

Ethylene‐dependent aerenchyma formation in adventitious roots is regulated differently in rice and maize

“…Furthermore, we found that ethylene biosynthesis and accumulation were significantly reduced in roots of the rcn1 mutant grown in stagnant conditions (i.e., stagnant, deoxygenated nutrient solution) (Yamauchi et al . ). Although inducible aerenchyma formation in adventitious roots of the rcn1 mutant is almost completely defective under stagnant conditions, aerenchyma still forms to some extent in the rcn1 roots under both aerated and stagnant conditions (Yamauchi et al .…”

“…Although inducible aerenchyma formation in adventitious roots of the rcn1 mutant is almost completely defective under stagnant conditions, aerenchyma still forms to some extent in the rcn1 roots under both aerated and stagnant conditions (Yamauchi et al . ). Interestingly, we also found that aerenchyma formation in roots of the rcn1 mutant is slightly less than that in the wild type, even under aerated conditions (Yamauchi et al .…”

“…Similarly, the expression levels of genes encoding ACSs and ACOs increase during inducible aerenchyma formation in roots of rice (Yamauchi et al . ) and maize (Geisler‐Lee et al . ), and the activities of these enzymes are enhanced during aerenchyma formation in maize roots under hypoxic conditions (He et al .…”

Focus on Ethylene

“…In the 2004 issue, two articles focused on specific downstream ethylene responses of shade avoidance and hyponastic growth. This issue features studies on aerenchyma formation (Yamauchi et al, 2015), root growth (Street et al, 2015), hypocotyl growth (Sun et al, 2015), hyponastic growth (Polko et al, 2015), abscission (Eccher et al, 2015), leaf senescence (Ueda and Kusaba, 2015), and the interaction of ethylene with light to regulate development (Weller et al, 2015). Of note, three articles in this issue emphasize a previously unheralded role for ethylene as an inhibitor of cell proliferation in both the shoot and root of Arabidopsis (Polko et al, 2015;Street et al, 2015;Tao et al, 2015).…”