Root cortical aerenchyma enhances nitrogen acquisition from low-nitrogen soils in maize

Abstract

Suboptimal nitrogen (N) availability is a primary constraint for crop production in developing nations, while in rich nations, intensive N fertilization carries substantial environmental and economic costs. Therefore, understanding root phenes that enhance N acquisition is of considerable importance. Structural-functional modeling predicts that root cortical aerenchyma (RCA) could improve N acquisition in maize (Zea mays). We evaluated the utility of RCA for N acquisition by physiological comparison of maize recombinant inbred lines contrasting in RCA grown under suboptimal and adequate N availability in greenhouse mesocosms and in the field in the United States and South Africa. N stress increased RCA formation by 200% in mesocosms and by 90% to 100% in the field. RCA formation substantially reduced root respiration and root N content. Under low-N conditions, RCA formation increased rooting depth by 15% to 31%, increased leaf N content by 28% to 81%, increased leaf chlorophyll content by 22%, increased leaf CO2 assimilation by 22%, increased vegetative biomass by 31% to 66%, and increased grain yield by 58%. Our results are consistent with the hypothesis that RCA improves plant growth under N-limiting conditions by decreasing root metabolic costs, thereby enhancing soil exploration and N acquisition in deep soil strata. Although potential fitness tradeoffs of RCA formation are poorly understood, increased RCA formation appears be a promising breeding target for enhancing crop N acquisition.

Figure 1.

Production of RCA as a percentage of cortical area in three root classes of maize harvested at 35 DAP under high-N and low-N conditions in soil mesocosms (GH2010). Data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05).

Figure 2.

Production of RCA between high-RCA and low-RCA maize RILs grown under high-N and low-N conditions and harvested at 35 DAP in soil mesocosms (GH) in 2010 and at 63 DAP in the field in South Africa (SA) and Pennsylvania (PA). The data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05) compared within each location.

Figure 3.

Negative correlation of root segment respiration with RCA in soil mesocosms (GH2010; r = −0.78, P < 0.001) and in the field (r = −0.85, P < 0.001).

Figure 4.

Specific root respiration (i.e. root respiration per unit of root length derived from the respiration of whole intact root systems) in high- and low-RCA genotypes at 35 DAP in both high- and low-N conditions in the mesocosms in 2010. Data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05).

Figure 5.

N stress reduced root segment respiration (A) and root N content (B) in second whorl crown roots in soil mesocosms (GH2013). RCA was negatively correlated with root respiration (r = −0.75, P < 0.05) and N content (r = −0.60, P < 0.05) under low-N conditions (C).

Figure 6.

Total root length of high- and low-RCA RILs at 35 DAP under high- and low-N conditions in mesocosms (GH2010). Data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05).

Figure 7.

D₉₅ of maize lines at 35 DAP in mesocosms (GH2010) and at 63 DAP in the field in South Africa (SA) under low-N conditions. Data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05) within the experiment.

Figure 8.

Chlorophyll concentration (A) and photosynthesis rate (B) of high- and low-RCA RILs at 35 DAP in both high- and low-N conditions in mesocosms (GH2010). Data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05).

Figure 9.

Relative shoot biomass under high-N and low-N conditions at 35 DAP in soil mesocosms (GH) in 2010 and at flowering (63 DAP) in the field in South Africa (SA) and Pennsylvania (PA). The data shown are means of four replicates ± se. Different letters represent significant differences (P < 0.05) compared within each location. Baseline values for shoot mass are as follows: GH = 1.77 g, SA = 75.28 g, and PA = 159.08 g.

Figure 10.

Correlation between yield and percentage of RCA (% cortex) under high-N (not significant) and low-N (r = 0.40, P = 0.05) conditions in the field in Pennsylvania.