Phytoglobins Improve Hypoxic Root Growth by Alleviating Apical Meristem Cell Death

Abstract

Hypoxic root growth in maize (Zea mays) is influenced by the expression of phytoglobins (ZmPgbs). Relative to the wild type, suppression of ZmPgb1.1 or ZmPgb1.2 inhibits the growth of roots exposed to 4% oxygen, causing structural abnormalities in the root apical meristems. These effects were accompanied by increasing levels of reactive oxygen species (ROS), possibly through the transcriptional induction of four Respiratory Burst Oxidase Homologs. TUNEL-positive nuclei in meristematic cells indicated the involvement of programmed cell death (PCD) in the process. These cells also accumulated nitric oxide and stained heavily for ethylene biosynthetic transcripts. A sharp increase in the expression level of several 1-aminocyclopropane synthase (ZmAcs2, ZmAcs6, and ZmAcs7), 1-aminocyclopropane oxidase (Aco15, Aco20, Aco31, and Aco35), and ethylene-responsive (ZmErf2 and ZmEbf1) genes was observed in hypoxic ZmPgb-suppressing roots, which overproduced ethylene. Inhibiting ROS synthesis with diphenyleneiodonium or ethylene perception with 1-methylcyclopropene suppressed PCD, increased BAX inhibitor-1, an effective attenuator of the death programs in eukaryotes, and restored root growth. Hypoxic roots overexpressing ZmPgbs had the lowest level of ethylene and showed a reduction in ROS staining and TUNEL-positive nuclei in the meristematic cells. These roots retained functional meristems and exhibited the highest growth performance when subjected to hypoxic conditions. Collectively, these results suggest a novel function of Pgbs in protecting root apical meristems from hypoxiainduced PCD through mechanisms initiated by nitric oxide and mediated by ethylene via ROS.Oxygen deficiency (hypoxia), experienced by plants grown in poorly drained soils or subjected to flooding, impairs plant growth and results in heavy crop losses (Dennis et al., 2000). Submergence or flooding reduces oxygen availability for plant cells, inhibiting the gas exchange required for basic physiological processes (Bailey-Serres and Voesenek, 2008). Both roots and shoots are affected by hypoxia, regardless of whether the plant is submerged or only the root is exposed to the condition. The consequences to shoots of prolonged root hypoxia include reduced photosynthetic rate and stomatal conductance, decreased leaf growth and senescence, wilting of the aboveground organs, and alterations in plant water relations (Mustroph and Albrecht, 2003). Ethylene accumulates rapidly in flooded Rumex palustris root cells (Visser et al., 1996), and in some species, ethylene affects the selective death of cortical cells generating lysogenous aerenchyma (Drew et al., 1979(Drew et al., , 2000; Drew, 1997) Precursors of ethylene have been shown to induce changes in Brassica napus growth behavior and root architecture (Patrick et al., 2009). Depending upon the concentration and species, ethylene can either stimulate or inhibit root growth (Konings and Jackson, 1979). Ethylene regulation of programmed cell death (PCD) is not restricted to hypoxia but, rather, is observed in ...

Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

“…This study shows that PGB1 is a key intermediate, linking ethylene signalling, via regulated NO removal, to O 2 sensing and hypoxia tolerance. This mechanism also provides a molecular explanation for the protective role of PGB1 during hypoxia and submergence described in prior studies 31,36–38 . Natural variation for ethylene-induced hypoxia adaptation was also observed in wild species and correlated with PGB1 induction 10 .…”

Group VII Ethylene Response Factors in Arabidopsis: Regulation and Physiological Roles

“…Reports regarding the influence of nitric oxide on a plant's ability to cope with hypoxia are controversial (Perazzolli et al, 2004;Gupta and Igamberdiev, 2016;Mira et al, 2016;Peng et al, 2016), making it hard to draw conclusions regarding the impact of the described regulation under hypoxia. However, ERF-VII behavior as novel NO sensors has made it possible to connect them to the physiology of this gaseous signal.…”

An NADPH Oxidase RBOH Functions in Rice Roots during Lysigenous Aerenchyma Formation under Oxygen-Deficient Conditions

“…In maize roots under hypoxic (oxygen-deficient) conditions, expression of genes encoding the A, B, C, and D isoforms of Zm-RBOH is stimulated during the cell death of the apical meristem (Mira et al, 2016). Previously, we found that waterlogging induces Zm-RBOHH expression in the cortical cells of primary roots at the same time it induces aerenchyma formation .…”