Distinct Molecular Biomechanical Mechanisms Inhibit Endosperm Cell-Wall Weakening and Seed Germination at Cold and Warm Nonoptimal Temperatures.

Temperature sensing to adjust developmental rates and phenological responses to different climatic environments is critical for plant survival. Population-based thermal-time threshold models predict linear relationships between temperature and, for example, seed germination rates (speed), but the mechanisms are not known. Here, we used an integrative approach into the molecular biomechanical mechanisms underpinning a thermal-time model by combining Lepidium sativum micropylar endosperm (CAP) and radicle transcriptome analysis at defined heat units (generated by different time-temperature combinations) with corresponding CAP biomechanics. The thermal-time model delivered linear relationships with germination rates, but the underpinning biomechanical mechanisms of CAP weakening differed fundamentally between the optimal (24°C-27°C), sub-optimal (colder: 11°C, 18°C) and supra-optimal (warmer: 32°C) temperatures. Chilling (11°C) differed from other temperatures in that its CAP weakening inhibition was combined with altered CAP stiffness/elasticity. Differentially expressed cell wall remodelling protein (CWRP) genes associated with CAP weakening and/or stiffness/elasticity were identified using defined heat unit comparisons. Xyloglucans, galactomannans, pectins and UDP-sugar metabolism were major targets. Temperature regulation of CAP CWRP expression by DELAY-OF-GERMINATION-1 (DOG1) controls CAP weakening and seed germination. We conclude that distinct and temperature-specific molecular and biomechanical mechanisms underpin the apparently linear thermal-time responses during CAP weakening and seed germination.