Aerenchyma in Maize and its relatives

Trends in Plant Science 3(6): 218-223 (1998)
Cell-death mechanisms in maize
Brent Buckner, Diane Janick-Buckner, John Gray and Guri S. Johal
   Aerenchyma production is common and extensive in the roots of prairie grasses such as eastern gamagrass (Tripsacum). Maize–Tripsacum hybrids have been produced in attempts to transfer the apomictic trait of Tripsacum to maize37. Coincidentally, the aerenchyma trait of Tripsacum was also transferred to maize, indicating that these two traits are linked in Tripsacum38. Because the organization of maize and Tripsacum chromosomes is similar, it is likely that the gene or genes that are involved in aerenchyma production can be more precisely mapped and ultimately isolated.

  1. Kindiger, B., Bai, D. and Sokolov, V. (1996) Assignment of gene(s) conferring apomixis in Tripsacum to a chromosome arm: cytological and molecular evidence, Genome 39, 1133-1141
  2. Comis, D. (1997) Aerenchyma: lifestyles for living under water, Agric. Res. 45, 4-8

Maydica 43:49, 1998.
Preliminary Survey of Root Aerenchyma in Tripsacum
Ray, J. D.; Kindiger, B.; Dewald, C. L.; Sinclair, T. R.
   Tripsacum plants of the species dactyloides (eastern gamagrass) have been observed to withstand flooded soil conditions and roots of this species have been observed to penetrate deep into heavy clay soils. One commonality between these conditions is the low oxygen environment surrounding the roots due to water logging or soil compression. In both cases, the presence of aerenchyma in T. dactyloides roots may have ameliorated the adverse impact of the low oxygen environment. Previously, we have found that some T. dactyloides accessions exhibit well-formed root aerenchyma even under well-aerated, non-stress environments which may allow a competitive advantage for this species in adapting to a wide range of habitats. In this survey of root anatomy, 15 of 16 species of Tripsacum were evaluated to determine the extent to which aerenchyma occur in a well-aerated, non-stress environment. Among the 15 species, 26 accessions were surveyed. In only five of the 15 species were large, well-formed aerenchyma found. This indicates that the ability to form aerenchyma under well-aerated, non-stress environments is not a universal adaptive mechanism within the genus and indicates the possibility of developing additional supraspecific groups based on root characteristics.

Plant and Soil 281:269–279 (2006)
Variation for root aerenchyma formation in flooded and non-flooded maize and teosinte seedlings
Y. Mano, F. Omori, T. Takamizo, B. Kindiger, R. McK. Bird & C. H. Loaisiga
   Morphological and anatomical factors such as aerenchyma formation in roots and the development of adventitious roots are considered to be amongst the most important developmental characteristics affecting flooding tolerance. In this study we investigated the lengths of adventitious roots and their capacity to form aerenchyma in three- and four-week-old seedlings of two maize (Zea mays ssp. mays, Linn.) inbred accessions, B64 and Na4, and one teosinte, Z. nicaraguensis Iltis & Benz (Poaceae), with and without a flooding treatment. Three weeks after sowing and following a seven day flooding treatment, both maize and teosinte seedlings formed aerenchyma in the cortex of the adventitious roots of the first three nodes. The degree of aerenchyma formation in the three genotypes increased with a second week of flooding treatment. In drained soil, the two maize accessions failed to form aerenchyma. In Z. nicaraguensis, aerenchyma developed in roots located at the first two nodes three weeks after sowing. In the fourth week, aerenchyma developed in roots of the third node, with a subsequent increase in aerenchyma in the second node roots. In a second experiment, we investigated the capacity of aerenchyma to develop in drained soil. An additional three teosinte species and 15 maize inbred lines, among them a set of flooding-tolerant maize lines, were evaluated. Evaluations indicate that accessions of Z. luxurians (Durieu & Asch. Bird) and two maize inbreds, B55 and Mo20W, form aerenchyma when not flooded. These materials may be useful genetic resources for the development of flooding-tolerant maize accessions.

Biologia Plantarum, 53(2): 263-270 (June 2009)
Aerenchyma formation in maize roots
Z. Lenochová, A. Soukup, O. Votrubová
   Maize (Zea mays L.) is generally considered to be a plant with aerenchyma formation inducible by environmental conditions. In our study, young maize plants, cultivated in various ways in order to minimise the stressing effect of hypoxia, flooding, mechanical impedance or nutrient starvation, were examined for the presence of aerenchyma in their primary roots. The area of aerenchyma in the root cortex was correlated with the root length. Although 12 different maize accessions were used, no plants without aerenchyma were acquired until an ethylene synthesis inhibitor was employed. Using an ACC-synthase inhibitor, it was confirmed that the aerenchyma formation is ethylene-regulated and dependent on irradiance. The presence of TUNEL-positive nuclei and ultrastructural changes in cortical cells suggest a connection between ethylene-dependent aerenchyma formation and programmed cell death. Position of cells with TUNEL-positive nuclei in relation to aerenchyma-channels was described.

Plant Cell Environ. 33(5):740-9. (2010 May)
Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.).
Zhu J, Brown KM, Lynch JP. Source Department of Horticulture, The Pennsylvania State University, University Park, PA 16802, USA. Abstract
   Root cortical aerenchyma (RCA) reduces root respiration in maize by converting living cortical tissue to air volume. We hypothesized that RCA increases drought tolerance by reducing root metabolic costs, permitting greater root growth and water acquisition from drying soil. To test this hypothesis, recombinant inbred lines with high and low RCA were observed under water stress in the field and in soil mesocosms in a greenhouse. In the field, lines with high RCA had 30% more shoot biomass at flowering compared with lines with low RCA under water stress. Root length density in deep soil was significantly greater in the high RCA lines compared with the low RCA lines. Mid-day leaf relative water content in the high RCA lines was 10% greater than in the low RCA lines under water stress. The high RCA lines averaged eight times the yield of the low RCA lines under water stress. In mesocosms, high RCA lines had less seminal root respiration, deeper rooting, and greater shoot biomass compared with low RCA lines under water stress. These results support the hypothesis that RCA is beneficial for drought tolerance in maize by reducing the metabolic cost of soil exploration.

Plant Signal Behav. 6(5): 759–761. (2011 May)
Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species
Takaki Yamauchi, Imene Rajhi, and Mikio Nakazono
   To adapt to waterlogging, maize (Zea mays) forms lysigenous aerenchyma in root cortex as a result of ethylene-promoted programmed cell death (PCD). Respiratory burst oxidase homolog (RBOH) gene encodes a homolog of gp91phox in NADPH oxidase, and has a role in the generation of reactive oxygen species (ROS). Recently, we found that during aerenchyma formation, RBOH was upregulated in all maize root tissues examined, whereas an ROS scavenging related metallothionein (MT) gene was downregulated specifically in cortical cells. Together these changes should lead to high accumulations of ROS in root cortex, thereby inducing PCD for aerenchyma formation. As further evidence of the involvement of ROS in root aerenchyma formation, the PCD was inhibited by diphenyleneiodonium (DPI), an NADPH oxidase inhibitor. Based on these results, we propose a model of cortical cell-specific PCD for root aerenchyma formation.

Plant Physiology 156(3): 1190-1201 (July 2011)
Root Cortical Aerenchyma Enhances the Growth of Maize on Soils with Suboptimal Availability of Nitrogen, Phosphorus, and Potassium
Johannes Auke Postma and Jonathan Paul Lynch
   Root cortical aerenchyma (RCA) is induced by hypoxia, drought, and several nutrient deficiencies. Previous research showed that RCA formation reduces the respiration and nutrient content of root tissue. We used SimRoot, a functional-structural model, to provide quantitative support for the hypothesis that RCA formation is a useful adaptation to suboptimal availability of phosphorus, nitrogen, and potassium by reducing the metabolic costs of soil exploration in maize (Zea mays). RCA increased the growth of simulated 40-d-old maize plants up to 55%, 54%, or 72% on low nitrogen, phosphorus, or potassium soil, respectively, and reduced critical fertility levels by 13%, 12%, or 7%, respectively. The greater utility of RCA on low-potassium soils is associated with the fact that root growth in potassium-deficient plants was more carbon limited than in phosphorus- and nitrogen-deficient plants. In contrast to potassium-deficient plants, phosphorus- and nitrogen-deficient plants allocate more carbon to the root system as the deficiency develops. The utility of RCA also depended on other root phenes and environmental factors. On low-phosphorus soils (7.5 µM), the utility of RCA was 2.9 times greater in plants with increased lateral branching density than in plants with normal branching. On low-nitrate soils, the utility of RCA formation was 56% greater in coarser soils with high nitrate leaching. Large genetic variation in RCA formation and the utility of RCA for a range of stresses position RCA as an interesting crop-breeding target for enhanced soil resource acquisition.

Plant Cell Environ. 2012 Sep;35(9):1618-30.
Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays).
Abiko, T., Kotula, L., Shiono, K., Malik, A.I., Colmer, T.D. and Nakazono, M.
   Enhancement of oxygen transport from shoot to root tip by the formation of aerenchyma and also a barrier to radial oxygen loss (ROL) in roots is common in waterlogging-tolerant plants. Zea nicaraguensis (teosinte), a wild relative of maize (Zea mays ssp. mays), grows in waterlogged soils. We investigated the formation of aerenchyma and ROL barrier induction in roots of Z. nicaraguensis, in comparison with roots of maize (inbred line Mi29), in a pot soil system and in hydroponics. Furthermore, depositions of suberin in the exodermis/hypodermis and lignin in the epidermis of adventitious roots of Z. nicaraguensis and maize grown in aerated or stagnant deoxygenated nutrient solution were studied. Growth of maize was more adversely affected by low oxygen in the root zone (waterlogged soil or stagnant deoxygenated nutrient solution) compared with Z. nicaraguensis. In stagnant deoxygenated solution, Z. nicaraguensis was superior to maize in transporting oxygen from shoot base to root tip due to formation of larger aerenchyma and a stronger barrier to ROL in adventitious roots. The relationships between the ROL barrier formation and suberin and lignin depositions in roots are discussed. The ROL barrier, in addition to aerenchyma, would contribute to the waterlogging tolerance of Z. nicaraguensis.