Comparative biomechanical and molecular mechanisms shaping erect and prostrate winter growth habits in wheat

The erect and prostrate growth habits are key plant architectural traits in wheat during the overwintering period. Interestingly, both erect and prostrate growth habits exhibit an erect phenotype during the seedling stage. However, during the overwintering period, wheat varieties with a prostrate growth habit transition from erect to prostrate, while those with an erect growth habit maintain their erect phenotype throughout. Generally, wheat varieties with an erect growth habit have weaker cold tolerance, whereas those with a prostrate growth habit exhibit stronger cold tolerance. These two growth habits have significant and distinctly different agronomic value across various production environments, yet their regulatory mechanisms remain unclear. This study was the first to integrate biomechanics with transcriptomics, unveiling the underlying mechanical regulatory mechanisms behind the erect and prostrate growth habits of wheat during the overwintering period from a biomechanical perspective. This study identified hardness, maximum shear force, shear forces do work, fiber properties, gravitational moment, center of gravity height, cohesiveness, and relative water content as key factors determining the differences in wheat growth habits. We propose that the erect growth habit follows a "structural rigidity reinforcement " strategy, characterized by lower tissue water content, suppression of the rise in the center of gravity height, and a synergistic increase in key mechanical properties such as hardness, springiness, shear resistance, and fiber characteristics. In contrast, the prostrate growth habit adopts a "structural flexibility adaptation" strategy, marked by higher relative water content, a rapid rise in the center of gravity height, increased gravitational moment, and reduced mechanical properties. A relationship analysis between the weighted gene co-expression network analysis (WGCNA) and these key traits identified 35 core candidate genes. Among them, 15, 6, and 14 genes showed significant correlations with hardness, fiber properties, and center of gravity height, respectively. These candidate genes are primarily involved in plant hormone signal transduction, auxin-activated signaling pathway, cell wall composition and synthesis, starch and sucrose metabolism, phenylpropanoid biosynthesis, and circadian rhythm-plant pathways. The mechanisms of these candidate genes and pathways require further investigation. We propose a coordinated network to explain the mechanistic regulatory strategies behind the erect and prostrate growth habits of wheat during the overwintering period. These findings provide a theoretical foundation for optimizing plant architecture and developing new varieties with robust structures and high yields.