Root cortical aerenchyma inhibits radial nutrient transport in maize (Zea mays)

Abstract

Background and aims: Formation of root cortical aerenchyma (RCA) can be induced by nutrient deficiency. In species adapted to aerobic soil conditions, this response is adaptive by reducing root maintenance requirements, thereby permitting greater soil exploration. One trade-off of RCA formation may be reduced radial transport of nutrients due to reduction in living cortical tissue. To test this hypothesis, radial nutrient transport in intact roots of maize (Zea mays) was investigated in two radiolabelling experiments employing genotypes with contrasting RCA.

Methods: In the first experiment, time-course dynamics of phosphate loading into the xylem were measured from excised nodal roots that varied in RCA formation. In the second experiment, uptake of phosphate, calcium and sulphate was measured in seminal roots of intact young plants in which variation in RCA was induced by treatments altering ethylene action or genetic differences.

Key results: In each of three paired genotype comparisons, the rate of phosphate exudation of high-RCA genotypes was significantly less than that of low-RCA genotypes. In the second experiment, radial nutrient transport of phosphate and calcium was negatively correlated with the extent of RCA for some genotypes.

Conclusions: The results support the hypothesis that RCA can reduce radial transport of some nutrients in some genotypes, which could be an important trade-off of this trait.

Keywords: Aerenchyma; Zea mays; calcium; maize; nutrient uptake; phosphorus; radial transport; root; sulfur.

Fig. 1.

Experimental setups for radionuclide application to root segments. (A) For experiment 1, a modified Pitman chamber was used to treat a 7·4-mm. segment of an excised first-whorl crown root. This top view of the acrylic glass chamber shows the 0·5 mL receiver compartment, where ³²P exudation from the cut end of the root was measured, the 1-mL treatment chamber where the ³²P was added, and the 1-mL leakage check compartment adjacent to the treatment compartment. The root tip was in a water bath containing unlabelled nutrient solution. Uptake of P was measured by adding the counts from the receiver compartment and those from the root segment inside it. (B) The chamber for experiment 2 permitted application of labelled nutrients to a 6-mm region of an intact maize seminal root. A 100-mL cup contained the whole plant, with the roots bathed in nutrient solution. One seminal root was inserted through two holes in a polypropylene tube, the openings were sealed with silicon grease and radionuclide solution was added to the tube.

Fig. 2.

Cross-sections from radionuclide-treated root segments from each genotype used in this study showing RCA formation. Images shown are representative of average RCA values for each treatment. The six images on the left are from experiment 1, where each side-by-side pair was studied at the same time, and the nine images on the right are from experiment 2, where each of the three treatments were compared at the same time. Scale bars = 400 μm.

Fig. 3.

Negative relationship between ³²P uptake and %RCA in six maize genotypes in experiment 1. The effect is significant at P < 0·0001.

Fig. 4.

Time course of cumulative ³²P exudation in three high-RCA genotypes (closed symbols) and three low-RCA genotypes (open symbols) in experiment 1. Error bars represent the s.e. RIL 360 is not visible because it is directly behind RIL 345.

Fig. 5.

Direct relationships between nutrient uptake and RCA in segments of intact maize seminal roots in experiment 2. (A) Calcium transport was negatively correlated with RCA formation in RIL 76 (r² = 0·337, P = 0·029, y = 0·359 − 2·87x). (B) Phosphate transport was negatively correlated with RCA formation in RIL 364 (r² = 0·388, P = 0·017, y = 2·59 − 0·923x). (C) A decreasing trend in sulphur transport was observed in RIL 39, although this was not significant (r² = 0·099, P = 0·204). Scale of ordinate axis is given as log + 1 to avoid negative values.