Specificity in root domain accumulation of Phytoglobin1 and nitric oxide (NO) determines meristematic viability in water-stressed Brassica napus roots

• Published in: Annals of botany 2023-04, Vol.131 (3), p.475-490
• Main Authors: Mira, Mohammed M, Ibrahim, Shimaa, So, Kenny, Kowatsch, Ralph, Duncan, Robert W, Hill, Robert D, Stasolla, Claudio
• Format: Article
• Language: English
• Subjects: Arabidopsis - physiology; Arabidopsis Proteins - genetics; Brassica napus - genetics; Brassinosteroids - metabolism; Dehydration - metabolism; Gene Expression Regulation, Plant; Indoleacetic Acids - metabolism; Meristem - metabolism; Nitric Oxide - metabolism; Original; Plant Roots - metabolism
• ISSN: 0305-7364; 1095-8290
• DOI: 10.1093/aob/mcac161

Drought reduces plant productivity, especially in the susceptible species Brassica napus. Water stress, mimicked by applications of 10 % polyethylene glycol (PEG), elevates nitric oxide (NO) in root cells after a few hours, contributing to degradation of the root apical meristems (RAMs), the function of which relies on auxin and brassinosteroids (BRs). Phytoglobins (Pgbs) are effective NO scavengers induced by this stress. This study examines the effects of BnPgb1 dysregulation in dehydrating B. napus roots, and the spatiotemporal relationship between Pgb1 and activities of auxin and BRs in the regulation of the RAM. Brassica napus lines over-expressing [BnPgb1(S)] or down-regulating [BnPgb1(RNAi)] BnPgb1 were exposed to PEG-induced water stress. The localization of BnPgb1, NO, auxin and PIN1 were analysed during the first 48 h, while the expression level of biosynthetic auxin and BR genes was measured during the first 24 h. Pharmacological treatments were conducted to assess the requirement of auxin and BR in dehydrating roots. During PEG stress, BnPgb1 protein accumulated preferentially in the peripheral domains of the root elongation zone, exposing the meristem to NO, which inhibits polar auxin transport (PAT), probably by interfering with PIN1 localization and the synthesis of auxin. Diminished auxin at the root tip depressed the synthesis of BR and caused the degradation of the RAMs. The strength of BnPgb1 signal in the elongation zone was increased in BnPgb1(S) roots, where NO was confined to the most apical cells. Consequently, PAT and auxin synthesis were retained, and the definition of RAMs was maintained. Auxin preservation of the RAM required BRs, although BRs alone was not sufficient to fully rescue drought-damaged RAMs in auxin-depleted environments. The tissue-specific localization of BnPgb1 and NO determine B. napus root responses to water stress. A model is proposed in which auxin and BRs act as downstream components of BnPgb1 signalling in the preservation of RAMs in dehydrating roots.