The StAR-related lipid transfer (START) domain containing proteins or START proteins, encoded by a plant amplified family of evolutionary conserved genes, play important roles in lipid binding, transport, signaling, and modulation of transcriptional activity in the plant kingdom, but there is limited information on their evolution, duplication, and associated sub- or neo-functionalization. Here we perform a comprehensive investigation of this family across the rice pangenome, using 10 wild and cultivated varieties. Conservation of START domains across all 10 rice genomes suggests low dispensability and critical functional roles for this family, further supported by chromosomal mapping, duplication and domain structure patterns. Analysis of synteny highlights a preponderance of segmental and dispersed duplication among STARTs, while transcriptomic investigation of the main cultivated variety Oryza sativa var. japonica reveals sub-functionalization amongst genes family members in terms of preferential expression across various developmental stages and anatomical parts, such as flowering. Ka/Ks ratios confirmed strong negative/purifying selection on START family evolution, implying that ontogeny recapitulated selection pressures during rice domestication. Our findings provide evidence for high conservation of START genes across rice varieties in numbers, as well as in their stringent regulation of Ka/Ks ratio, and showed strong functional dependency of plants on START proteins for their growth and reproductive development. We believe that our findings advance the limited knowledge about plant START domain diversity and evolution, and pave the way for more detailed assessment of individual structural classes of START proteins among plants and their domain specific substrate preferences, to complement existing studies in animals and yeast.
Global warming exhibits profound effects on plant fitness and productivity. To withstand stress, plants sacrifice their growth and activate protective stress responses for ensuring survival. However, the switch between growth and stress is largely elusive. In the past decade, emerging role of Target of Rapamycin (TOR) has been studied linking energy and stress signaling. Here, we have identified an important role of Glc-TOR signaling in plant adaptation to heat stress (HS). We show that Glc-TOR signaling regulates thermotolerance and thermomemory response through distinct mechanisms. Glc-TOR via E2Fa signaling module governs the transcriptome reprogramming of a myriad set of genes involved in HS protection and recovery. Glc also epigenetically governs the transcription of core HS signaling genes in a TOR-dependent manner. TOR acts in concert with p300/CREB HISTONE ACETYLTRANSFERASE1 (HAC1) and dictates the epigenetic landscape of HS loci to regulate thermotolerance. Arabidopsis plants defective in TOR and HAC1 exhibited reduced thermotolerance with a decrease in expression of core HS signaling genes. TOR also promotes accumulation of histone H3K4me3 marks at the promoters of thermomemory-related genes and therefore, governs thermomemory. Further, genome-wide transcriptome of Glc-TOR shows huge overlap with targets of chromatin remodeler BRAHMA, especially with genes enriched in stress, chromatin remodelling and histone/protein modifications. Collectively, our findings thus reveal a mechanistic framework in which Glc-TOR signalling through multiple modules determines the integration of stress and energy signaling to regulate thermotolerance and thermomemory.
Global warming exhibits profound effects on plant fitness and productivity. To withstand stress, plants sacrifice their growth and activate protective stress responses for ensuring survival. However, the switch between growth and stress is largely elusive. In the past decade, the role of the target of rapamycin (TOR) linking energy and stress signalling is emerging. Here, we have identified an important role of Glucose (Glc)-TOR signalling in plant adaptation to heat stress (HS). Glc via TOR governs the transcriptome reprogramming of a large number of genes involved in heat stress protection. Downstream to Glc-TOR, the E2Fa signalling module regulates the transcription of heat shock factors through direct recruitment of E2Fa onto their promoter regions. Also, Glc epigenetically regulates the transcription of core HS signalling genes in a TOR-dependent manner. TOR acts in concert with p300/CREB HISTONE ACETYLTRANSFERASE1 (HAC1) and dictates the epigenetic landscape of HS loci to regulate thermotolerance. Arabidopsis plants defective in TOR and HAC1 exhibited reduced thermotolerance with a decrease in the expression of core HS signalling genes. Together, our findings reveal a mechanistic framework in which Glc-TOR signalling through different modules integrates stress and energy signalling to regulate thermotolerance.
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