Root Cortical Aerenchyma Enhances Nitrogen Acquisition from Low-Nitrogen Soils in Maize

Abstract

ORCID ID: 0000-0002-7265-9790 (J.P.L.).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 CO 2 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.

Functional implications of root cortical senescence for soil resource capture

“…Root cortical phenes are important for plant performance, particularly under edaphic stress (Zhu et al 2010;Chimungu et al 2014a;Chimungu et al 2014b;Saengwilai et al 2014;Schneider et al 2017b). Root phenes that reduce root metabolic costs including RCS, RCA, cortical cell file number, and cortical cell size reduce carbon and nutrient costs for soil exploration (Chimungu et al 2014a;Lynch et al 2014;Saengwilai et al 2014;Chimungu et al 2014b;Schneider et al 2017a).…”

“…Both RCS and RCA are accelerated by nutrient deficiencies (Gillespie and Deacon 1988;Drew et al 1989;Elliott et al 1993), reduce radial nutrient transport (Hu et al 2014;Schneider et al 2017a), reduce radial hydraulic conductivity (Fan et al 2007;Schneider et al 2017a), reduce metabolic costs (Zhu et al 2010;Postma and Lynch 2011b;Jaramillo et al 2013;Saengwilai et al 2014;Chimungu et al 2015), are influenced by exposure to ethylene (Lascaris and Deacon 1991b;Lenochová et al 2009;Schneider et al 2017c), and are types of PCD Jiang et al 2010;Schneider et al 2017c). Two ethylene-related genes were upregulated during both RCS and RCA formation (Rajhi et al 2011;Schneider et al 2017c).…”

“…Root phenes that reduce root metabolic costs including RCS, RCA, cortical cell file number, and cortical cell size reduce carbon and nutrient costs for soil exploration (Chimungu et al 2014a;Lynch et al 2014;Saengwilai et al 2014;Chimungu et al 2014b;Schneider et al 2017a). RCS is a promising breeding target for improved soil resource acquisition.…”

“…Cortical phene states that reduce living cortical tissue reduce root respiration and nutrient content, thereby permitting greater resource allocation to other plant functions including growth and reproduction Lynch 2015). For example, the development of root cortical aerenchyma (RCA) in maize improves plant performance in environments with suboptimal nutrient and water availability (Zhu et al 2010;Postma and Lynch 2011a, b;Jaramillo et al 2013;Saengwilai et al 2014;Chimungu et al 2015), an effect which modeling studies show can be attributed to a reduction in root metabolic costs (Postma et al 2014;Dathe et al 2016). Fewer cell files or greater cell size in the root cortex of maize substantially reduces root respiration and improves soil exploration and water acquisition in conditions of suboptimal water availability (Chimungu et al 2014a(Chimungu et al , 2014b.…”

OpenSimRoot: widening the scope and application of root architectural models

“…A. Postma, T. Wojciechowski, C. Kuppe, J. P. Lynch, unpublished) simulated the root class‐ and time‐dependent formation of RCA and root cortical senescence (RCS), respectively, and determined that RCA and RCS may be mechanisms underlying greater growth on low‐nutrient soils in maize, bean and barley, possibly via efficient use and recycling of resources. Genotypic contrast studies on low‐N soils concur with these simulation results (Saengwilai et al ., 2014), which suggests that O pen S im R oot can be used to scale up from anatomy to crop stands.…”