Transcriptome-metabolome and anatomy conjoint analysis of vital component change of photosynthesis of Foxtail millet under different drought conditions

Drought caused by extreme climate change has become more severe and unpredictable, causing imperceptible effects on leaf photosynthesis in foxtail millet. To investigate the damage, we performed light drought (LD) and heavy drought (HD) treatments at both the elongation (Y) and booting stages to obtain a comprehensive understanding of the morphological, anatomical, physiological, transcriptome, and metabolome levels. Under drought stress, the length and area of leaves decreased, especially during the HD treatment at the booting stage. The number of mesophyll cells and the area of large vascular bundles were both decreased under LD and HD treatments at the booting stage, as well as with more blurring vascular bundle structure and Kranz anatomy. However, these numbers decreased but with no significance under Y-LD and Y-HD treatments at the elongation stage. The net photosynthetic rate, stomatal conductivity, transpiration rate, and intercellular CO2 concentration significantly decreased at the booting stage. In addition, the efficiency of electron transfers in photosystem II (PS II) decreased. Conjunction analyses of the transcriptome and metabolome were utilized to uncover the underlying mechanism at the booting stage. The results showed that there was no common differentially enriched pathway in the transcriptome and metabolome under LD treatment but thirty-two pathways were enriched in both the transcript and metabolome under HD treatment. Among these, three pathways arginine, proline metabolism, tyrosine metabolism, ubiquinone, and other terpenoid-quinone biosynthesis pathways were differentially enriched in both the transcript and metabolome. The accumulation of Homogentisate, Salidroside, Homoprotocatechuate, L-DOPA, Tyramine, and L-Tyrosine increased under drought stress. Although genes related to PSII and the Calvin cycle were slightly up-regulated under LD conditions, they were down-regulated under HD condition. The metabolites of Ribose-5P, Glycerate-3P, D-Fructosel 1,6P2, and D-Fructose-6P were all decreased in both the LD and HD treatments, especially D-Fructose-6P, confirming that drought stress had a negative effect on the Calvin cycle. The results revealed that regardless of the severity of drought, photosynthetic function was compromised not only at the morphological and anatomical levels but also in terms of impaired ATP synthase and inhibited photosynthetic CO2 assimilation.