Large Root Cortical Cell Size Improves Drought Tolerance in Maize

Abstract

ORCID ID: 0000-0002-7265-9790 (J.P.L.).The objective of this study was to test the hypothesis that large cortical cell size (CCS) would improve drought tolerance by reducing root metabolic costs. Maize (Zea mays) lines contrasting in root CCS measured as cross-sectional area were grown under well-watered and water-stressed conditions in greenhouse mesocosms and in the field in the United States and Malawi. CCS varied among genotypes, ranging from 101 to 533 mm 2 . In mesocosms, large CCS reduced respiration per unit of root length by 59%. Under water stress in mesocosms, lines with large CCS had between 21% and 27% deeper rooting (depth above which 95% of total root length is located in the soil profile), 50% greater stomatal conductance, 59% greater leaf CO 2 assimilation, and between 34% and 44% greater shoot biomass than lines with small CCS. Under water stress in the field, lines with large CCS had between 32% and 41% deeper rooting (depth above which 95% of total root length is located in the soil profile), 32% lighter stem water isotopic ratio of 18 O to 16 O signature, signifying deeper water capture, between 22% and 30% greater leaf relative water content, between 51% and 100% greater shoot biomass at flowering, and between 99% and 145% greater yield than lines with small cells. Our results are consistent with the hypothesis that large CCS improves drought tolerance by reducing the metabolic cost of soil exploration, enabling deeper soil exploration, greater water acquisition, and improved growth and yield under water stress. These results, coupled with the substantial genetic variation for CCS in diverse maize germplasm, suggest that CCS merits attention as a potential breeding target to improve the drought tolerance of maize and possibly other cereal crops.

Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition

“…These results support growing evidence that root phenes and phene states that reduce the metabolic cost of soil exploration are adaptive in resource-poor soil environments (Chimungu et al, 2014a(Chimungu et al, , 2014b(Chimungu et al, , 2015Saengwilai et al, 2014;Lynch, 2015;Miguel et al, 2015;Schneider et al, 2017). In this context, root anatomical phenes merit attention as breeding targets for more stress-tolerant crops.…”

Functional implications of root cortical senescence for soil resource capture

“…The identification of genetic markers controlling RCS would greatly facilitate their use in breeding programs (Lynch 2011;Henry et al 2012;York et al 2013). Advances in laser ablation tomography may enable the phenotyping of root anatomical traits on targeted root segments in a high-throughput manner (Chimungu et al 2014a;Saengwilai et al 2014;Chimungu et al 2014b). However, since RCS changes temporally and spatially on a root system and varies by root class, the analysis of several root segments on the same root or threedimensional imaging may be necessary.…”

“…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).…”

“…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.…”

“…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. Recently, root cortical senescence (RCS), a phene anatomically distinct from RCA, has also been identified as a root phene that reduces root metabolic costs, thereby improving plant growth under suboptimal nutrient availability.…”