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In their natural habitats, seagrasses face multiple abiotic stressors, which can often occur simultaneously. However, most studies have only focused on growth and physiological responses to single stressors. Here, we examined transcriptome responses of the tropical seagrass Halophila stipulacea collected from a northern Gulf of Aqaba pristine site and an anthropogenically-impacted site, grown in a mesocosm, and exposed to ecologically-relevant, single and combined, thermal and excess nutrient stressors. Growth of plants from the impacted site was more tolerant to stress than plants from the pristine site. The combined thermal and nutrient stressor elicited greater transcriptome reprogramming than the single stressors in both populations and induced the expression of a combination-specific set of genes involved in stress responses. Furthermore, thermal stress exerted a dominant influence upon the transcriptome response to the combined stressor. Transcriptomes of plants from the impacted site displayed reduced responsiveness to stress, the presence of genes exhibiting a “stress-ready” mode of expression under all stressors, and increased resilience (recovery to control transcriptomes). We also identified core stress-response genes that could be leveraged as early indicators of stress in the field. Overall, our data suggest that environmental conditions in seagrass habitats can drive local molecular adaptation, and that the response of seagrasses to combined stressors associated with climate change and coastal anthropogenic stressors cannot be predicted from the response to single stressors. 

Abstract Translation of psbA, the chloroplast gene that encodes the D1 subunit of Photosystem II (PSII), is important for both PSII biogenesis and repair. The translation of the psbA transcript in the chloroplast is under the control of nuclear gene products. Using a Chlamydomonas forward genetic screen and whole genome sequencing, we found a mutant defective in PSII activity and mapped the causative gene to be the homolog of Arabidopsis High Chlorophyll Fluorescence 244 (HCF244) gene, or CrHCF244. We then demonstrated that CrHCF244 is required for psbA translation in the alga, consistent with the function of HCF244 in Arabidopsis. The Arabidopsis HCF244 gene also partially complemented the algal mutant. These results experimentally support the functional conservation of the homologs in green algae and land plants. Intriguingly, the CrHCF244 mutant also exhibited a relatively high rate of suppressor mutants, pointing to the presence of alternative factor(s)/pathway(s) for D1 translation control. The establishment of CrHCF244 as a psbA translation factor in Chlamydomonas showed the similarities in psbA translation regulation in algae and plants. The future identification of the alternative factor(s) in this alga will provide insights on psbA translation in plants.