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Most epiphytes are found in low-nutrient environments with an intermittent water supply. To deal with water limitation, many bromeliads perform crassulacean acid metabolism (CAM), such as  Guzmania monostachia , which shifts from C 3  to CAM and can recycle CO 2  from the respiration while stomata remain closed during daytime and nighttime (CAM-idling mode). Since the absorbing leaf trichomes can be in contact with organic (urea) and inorganic nutrients (NO 3  − , NH 4  + ) and the urea hydrolysis releases NH 4  +  and CO 2 , we hypothesized that urea can integrate the N and C metabolism during periods of severe drought. Under this condition, NH 4  +  can be assimilated into amino acids through glutamine synthetase (GS), while the CO 2  can be pre-fixated by phosphoenolpyruvate carboxylase (PEPC). In this context, we evaluated the foliar transcriptome of  G. monostachia  to compare the relative gene expression of some genes involved with CAM and the N metabolism when bromeliads were submitted to 7days of drought. We also conducted a controlled experiment with an extended water deficit period (21days) in which bromeliads were cultivated in different N sources (urea, NH 4  + , and NO 3  − ). Our transcriptome results demonstrated an increment in the expression of genes related to CAM, particularly those involved in the carboxylation metabolism ( PEPC1 ,  PPCK , and  NAD-MDH ), the movement of malate through vacuolar membrane ( ALMT9 ), and the decarboxylation process ( PEPCK ). Urea stimulated the expression of  PEPC1  and  ALMT9 , while  Urease  transcripts increased under water deficit. Under this same condition,  GS1  gene expression increased, indicating that the NH 4  +  from urea hydrolysis can be assimilated in the cytosol. We suggest that the link between C and N metabolism occurred through the supply of carbon skeleton (2-oxoglutarate, 2-OG) by the cytosolic isocitrate dehydrogenase since the number of  NADP - ICDH  transcripts was also higher under drought conditions. These findings indicate that while urea hydrolysis provides NH 4  +  that can be consumed by glutamine synthetase-cytosolic/glutamate synthase (GS1/GOGAT) cycle, the CO 2  can be used by CAM, maintaining photosynthetic efficiency even when most stomata remain closed 24h (CAM-idling) as in the case of a severe water deficit condition. Thus, we suggest that urea could be used by  G. monostachia  as a strategy to increase its survival under drought, integrating N and C metabolism.

frontiers in plant science

Transcriptomic and Biochemical Analysis Reveal Integrative Pathways Between Carbon and Nitrogen Metabolism in Guzmania monostachia (Bromeliaceae) Under Drought