C ₄ photosynthesis in the rice paddy: Insights from the Noxious Weed Echinochloa glabrescens

The C ₄ pathway is a highly complex trait that increases photosynthetic efficiency in more than 60 plant lineages. Although the majority of C ₄ plants occupy disturbed, arid, and nutrient-poor habitats, some grow in high-nutrient, waterlogged conditions. One such example is Echinochloa glabrescens, which is an aggressive weed of rice paddies. We generated comprehensive transcriptome datasets for C ₄ E. glabrescens and C ₃ rice to identify genes associated with adaption to waterlogged, nutrient-replete conditions, but also used the data to better understand how C ₄ photosynthesis operates in these conditions. Leaves ofE. glabrescens exhibited classical Kranz anatomy with lightly lobed mesophyll cells having low chloroplast coverage. As with rice and other hygrophytic C ₃species, leaves of E. glabrescens accumulated a chloroplastic phosphoenolpyruvate carboxylase protein, albeit at reduced amounts relative to rice. The arid-grown species Setaria italica (C ₄) and Brachypodium distachyon (C ₃) were also found to accumulate chloroplastic phosphoenolpyruvate carboxylase. We identified a molecular signature associated with C ₄ photosynthesis in nutrient-replete, waterlogged conditions that is highly similar to those previously reported from C ₄ plants that grow in more arid conditions. We also identified a cohort of genes that have been subjected to a selective sweep associated with growth in paddy conditions. Overall, this approach highlights the value of using wild species such as weeds to identify adaptions to specific conditions associated with high-yielding crops in agriculture.