Abstract
Variations of photosynthetic structures in different tissues or cells are in coordination with changes in various aspects, e.g. physiology, biochemistry, gene expression, etc. Most C4 plant species undergo developmental enhancement of the photosynthetic system, which may present different modes of changes between anatomy and physiology/biochemistry. In the current study, we investigated a Kranz-type C4 species Salsola ferganica with the progressive development of photosynthetic (PS) structure, performance of PS physiology, induction of PS enzymes, and transcriptional and translational regulation of PS genes, results revealed that S. ferganica presented C3 type anatomy in cotyledons but C4 type in leaves (C3/L4), with the C4 system separation of initial carbon fixation in the palisade mesophyll (M) cells and the following incorporation into triosephosphates and sugars in the bundle sheath (BS) cells, respectively. The BS cells continuously surrounded the vascular bundles and water storage cells in leaf anatomic structure. Compared to the single-cell C4 species Suaeda aralocaspica, S. ferganica exhibited similar developmental enhancement of C4 syndrome temporally and spatially in anatomic structures, enzyme activities, and gene expression, which suggests that completion of differentiation of the photosynthetic system is necessary for a C4 assimilation pathway. Besides, S. ferganica also displayed some different characteristics compared to S. aralocaspica in photosynthetic physiology, e.g. a more flexible δ13C value, much lower phosphoenolpyruvate carboxylase (PEPC) activity, and an insensitive response to stimuli, etc., which were not typical C4 characteristics. We speculate that this may suggest a different status of these two species in the evolutionary process of the photosynthesis pathway. Our findings will contribute to further understanding of the diversity of photosynthesis systems in Kranz-type C4 species and the Salsola genus.
Highlights
Photosynthetic carbon assimilation pathways at least include C3, C4, CAM (Crassulacean acid metabolism), and/or C2 (C3-C4 intermediate) types (Raghavendra and Das, 1993; Khoshravesh et al, 2016), each is associated with distinct features of leaf anatomy, physiology, biochemistry, etc. (Sage and Stata, 2015)
Based on our observations and updates on the Salsola genus, and by employing SC-C4 plant species S. aralocaspica as the control, in the present study, we address the following questions: (1) Does the photosynthetic anatomy in S. ferganica become optimized with plant development progression and if so how does it change? (2) How do the physiology and biochemistry processes progress in coordination with photosynthetic structure differentiation? (3) What photosynthetic enzymes and genes act in the process? By addressing these questions, our findings expand our knowledge of the phenomenon of developmental enhancement of the C4 system in S. ferganica and increase our understanding of the physiology and biochemistry of carbon fixation in photosynthetic pathways
We found that the dynamics of trichome growth and decline on plants were corresponding to the development rhythms of S. ferganica, i.e. trichomes were thick and long at an early stage while shorter and thinner at a later stage, which suggests that trichomes must be an adaptive structure to protect seedling survival
Summary
Photosynthetic carbon assimilation pathways at least include C3, C4, CAM (Crassulacean acid metabolism), and/or C2 (C3-C4 intermediate) types (Raghavendra and Das, 1993; Khoshravesh et al, 2016), each is associated with distinct features of leaf anatomy, physiology, biochemistry, etc. (Sage and Stata, 2015). Four SC-C4 terrestrial species have been recorded, i.e. Bienertia sinuspersici, Bienertia Cycloptera, Bienertia kavirense, and Suaeda aralocaspica, all belonging to the Amaranthaceae (Chenopodiaceae before), which have different spatial distributions of organelles and photosynthetic enzymes in a single chlorenchyma cell (Lung et al, 2012). Behaviors (distribution, activity, etc.) of photosynthetic enzymes in single cells will be correspondingly changed with the structural adjustment (Voznesenskaya et al, 2001a). These variations of photosynthetic anatomy and enzyme function may promote a deeper understanding of carbon assimilation pathway in plants
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