Regulation of Root Elongation under Phosphorus Stress Involves Changes in Ethylene Responsiveness

Abstract

We characterized the growth of the primary root of Arabidopsis under phosphorus sufficiency (1 mm phosphate) and deficiency (1 m phosphate), focusing on the role of ethylene. We quantified the spatial profile of relative elongation with a novel method based on image processing, as well as the production rates of cortical cells, trichoblasts, and atrichoblasts. Phosphorus deficiency moderately decreased the maximal rate of relative elongation, shortened the growth zone, and decreased the production rate of both epidermal cell types but not of cortical cells. Inhibiting ethylene production (with aminoethoxyvinyl-glycine) or action (with 1-methylcyclopropene) increased elongation in high phosphorus and decreased it in low phosphorus. That these effects were specific to ethylene was confirmed by negating the effect of inhibited ethylene production with simultaneous treatment with an ethylene precursor (1-aminocyclopropane-1-carboxylic acid). Under both phosphorus regimes, ethylene regulated the maximal rate of relative elongation rather than the size of the growth zone. In addition, inhibiting ethylene action in high versus low phosphorus elicited opposite responses for the position of root hair initiation and for the production rates of cortex cells and atrichoblasts. We conclude that the root system acclimates to phosphorus deficiency by changing the signal transduction pathway connecting ethylene levels to growth and division.Plant root systems display an array of physiological, morphological, and architectural responses to low phosphorus availability. These responses enhance the ability of the root to explore the soil and include changes in branching patterns, in elongation rate, and in root hair length and density (Bates and Lynch, 1996;Bonser et al., 1996;Borch et al., 1999; Lynch and Brown, 2001; Ma et al., 2001a). These changes accompany changes in biochemical and metabolic processes and both together presumably represent adaptive responses to assist growth during phosphorus deficiency. In particular, the growth of root hairs and their response to phosphorus availability is important in the acquisition of this highly immobile nutrient (Lewis and Quirk, 1967;Bhat and Nye, 1974;Gahoonia and Nielsen, 1997; Lynch, 2000a, 2000b; Ma et al., 2001b).In response to low phosphorus, adaptive changes in roots may be mediated through the plant hormone ethylene. Both phosphorus deficiency and ethylene cause similar changes in root systems, such as aerenchyma formation, altered root growth angle, and stimulated root hair development (He et al., 1992;Lynch and Brown, 1997;Borch et al., 1999; Lynch and Brown, 2001). In bean (Phaseolus vulgaris), ethylene inhibits root elongation in phosphorus-sufficient conditions but maintains elongation under phosphorus deficiency (Borch et al., 1999). This finding suggests that roots respond to phosphorus stress by changing ethylene signal transduction pathways involved in regulating growth.In this report, we focus on the role of ethylene in mediating growth responses to low phosphoru...

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

“…Elongation rate is truncated apically, as also reported over time for wild-type roots responding to saturating oryzalin and for mor1 roots responding to a shift in temperature (Sugimoto et al, 2003). Because elongation zones are truncated apically when a root responds to deficits of water (Sharp et al, 1988) and phosphorus (Ma et al, 2003), we postulate that the truncation of the elongation rate profile reflects a response to stress, whereas the stimulation of tangential expansion is specific to the disruption of microtubule function.…”

Acclimation to soil flooding — sensing and signal-transduction

“…Analogously, low phosphorus increased the sensitivity of root elongation in Arabidopsis thaliana to ethylene (Ma et al, 2003). Aerenchyma formation does not appear to be exclusively induced by low phosphorus and nitrogen, since Bouranis et al (2003) found similar responses in sulphate-starved maize plants.…”

Longitudinal zonation pattern inArabidopsisroot tip defined by a multiple structural change algorithm

“…The rootward border of the DZ corresponds to the position at which cell elongation ceases (van der Weele et al, 2003;Ivanov and Dubrovsky, 2013). Therefore, identification of the boundary between the EZ and DZ is straightforward and is based on either cell length profile data or the appearance of the first root hair bulges, which is a hallmark of termination of elongation (Dolan et al, 1993;Ma et al, 2003;Dolan and Davies, 2004). Despite the importance of being able to fully characterize the apical-basal patterning of the root tip, no consensus on the domains and zones in the arabidopsis root apex has been attained (Ivanov and Dubrovsky, 2013).…”