Evidence for within‐species transition between drought response strategies in Nicotiana benthamiana

• Published in: The New phytologist 2024-10, Vol.244 (2), p.464-476
• Main Authors: Asadyar, Leila, Felippes, Felipe Fenselau, Bally, Julia, Blackman, Chris J., An, Jiyuan, Sussmilch, Frances C., Moghaddam, Lalehvash, Williams, Brett, Blanksby, Stephen J., Brodribb, Timothy J., Waterhouse, Peter M.
• Format: Article
• Language: English
• Subjects: Alkanes; Alkanes - metabolism; arid habitats; Australia; Biosynthesis; Composition; Cuticles; Cuticular wax; cuticular wax composition; Drought; drought responses; Droughts; Environmental control; Epicuticular wax; Flowering; Flowers - anatomy & histology; Flowers - physiology; Gene expression; gene expression profiles; Gene Expression Regulation, Plant; Genes, Plant; Geographical distribution; Life cycle; Nicotiana - genetics; Nicotiana - physiology; Nicotiana benthamiana; Permeability; Phenotype; phenotypic responses; physiological responses; Plant cuticle; Plant Epidermis - physiology; Plant Leaves - anatomy & histology; Plant Leaves - physiology; Species Specificity; Stress, Physiological; Water - metabolism; Water deprivation; Water loss; Water stress; Waxes; Waxes - metabolism
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.19898

Summary Nicotiana benthamiana is predominantly distributed in arid habitats across northern Australia. However, none of six geographically isolated accessions shows obvious xerophytic morphological features. To investigate how these tender‐looking plants withstand drought, we examined their responses to water deprivation, assessed phenotypic, physiological, and cellular responses, and analysed cuticular wax composition and wax biosynthesis gene expression profiles. Results showed that the Central Australia (CA) accession, globally known as a research tool, has evolved a drought escape strategy with early vigour, short life cycle, and weak, water loss‐limiting responses. By contrast, a northern Queensland (NQ) accession responded to drought by slowing growth, inhibiting flowering, increasing leaf cuticle thickness, and altering cuticular wax composition. Under water stress, NQ increased the heat stability and water impermeability of its cuticle by extending the carbon backbone of cuticular long‐chain alkanes from c. 25 to 33. This correlated with rapid upregulation of at least five wax biosynthesis genes. In CA, the alkane chain lengths (c. 25) and gene expression profiles remained largely unaltered. This study highlights complex genetic and environmental control over cuticle composition and provides evidence for divergence into at least two fundamentally different drought response strategies within the N. benthamiana species in