Within-individual phenotypic plasticity in flowers fosters pollination niche shift

Authors thank Raquel Sánchez, Angel Caravante, Isabel Sánchez Almazo, Tatiana López Pérez, Samuel Cantarero, María José Jorquera and Germán Fernández for helping us during several phases of the study and Iván Rodríguez Arós for drawing the insect silhouettes. This research is supported by grants from the Spanish Ministry of Science, Innovation and Universities (CGL2015-71634-P, CGL2015-63827-P, CGL2017-86626-C2-1-P, CGL2017- 86626-C2-2-P, UNGR15-CE-3315, including EU FEDER funds), Junta de Andalucía (P18- FR-3641), Xunta de Galicia (CITACA), BBVA Foundation (PR17_ECO_0021), and a contract grant to C.A. from the former Spanish Ministry of Economy and Competitiveness (RYC-2012-12277). This is a contribution to the Research Unit Modeling Nature, funded by the Consejería de Economía, Conocimiento, Empresas y Universidad, and European Regional Development Fund (ERDF), reference SOMM17/6109/UGR.Phenotypic plasticity, the ability of a genotype of producing different phenotypes when exposed to different environments, may impact ecological interactions. We study here how within-individual plasticity in Moricandia arvensis flowers modifies its pollination niche. During spring, this plant produces large, cross-shaped, UV-reflecting lilac flowers attracting mostly long-tongued large bees. However, unlike most co-occurring species, M. arvensis keeps flowering during the hot, dry summer due to its plasticity in key vegetative traits. Changes in temperature and photoperiod in summer trigger changes in gene expression and the production of small, rounded, UV-absorbing white flowers that attract a different assemblage of generalist pollinators. This shift in pollination niche potentially allows successful reproduction in harsh conditions, facilitating M. arvensis to face anthropogenic perturbations and climate change. Floral phenotypes impact interactions between plants and pollinators. Here, the authors show that Moricandia arvensis displays discrete seasonal plasticity in floral phenotype, with large, lilac flowers attracting long-tongued bees in spring and small, rounded, white flowers attracting generalist pollinators in summer.Spanish Ministry of Science, Innovation and Universities (EU FEDER funds) CGL2015-71634-P CGL2015-63827-P CGL2017-86626-C2-1-P CGL2017-86626-C2-2-P UNGR15-CE-3315Junta de Andalucia P18-FR-3641Xunta de GaliciaBBVA Foundation PR17_ECO_0021Spanish Ministry of Economy and Competitiveness RYC-2012-12277Consejeria de Economia, Conocimiento, Empresas y Universidad SOMM17/6109/UGREuropean Union (EU) SOMM17/6109/UG

A simple mechanism for the establishment of C2‐specific gene expression in Brassicaceae

The transition of C3, via C2&nbsp;towards C4&nbsp;photosynthesis is an important example of stepwise evolution of a complex genetic trait. A common feature that was gradually emphasized during this trajectory is the evolution of a CO2&nbsp;concentration mechanism around Rubisco. In C2&nbsp;plants, this mechanism is based on tissue‐specific accumulation of glycine decarboxylase (GDC) in bundle sheath (BS) cells, relative to global expression in the cells of C3&nbsp;leaves. This limits photorespiratory CO2&nbsp;release to BS cells. Because BS cells are surrounded by photosynthetically active mesophyll cells, this arrangement enhances the probability of re‐fixation of CO2. The restriction of GDC to BS cells was mainly achieved by confinement of its P‐subunit (GLDP). Here, we provide a mechanism for the establishment of C2‐type gene expression by studying the upstream sequences of C3&nbsp;Gldp&nbsp;genes in&nbsp;Arabidopsis thaliana. Deletion of 59&nbsp;bp in the upstream region of&nbsp;AtGldp1&nbsp;restricted expression of a reporter gene to BS cells and the vasculature without affecting diurnal variation. This region was named the &lsquo;M box&rsquo;. Similar results were obtained for the&nbsp;AtGldp2&nbsp;gene. Fusion of the M box to endogenous or exogenous promoters supported mesophyll expression. Nucleosome densities at the M box were low, suggesting an open chromatin structure facilitating transcription factor binding.&nbsp;In silico&nbsp;analysis defined a possible consensus for the element that was conserved across the Brassicaceae, but not in&nbsp;Moricandia nitens, a C2&nbsp;plant. Collective results provide evidence that a simple mutation is sufficient for establishment of C2‐specific gene expression in a C3&nbsp;plant.</p

Loss of the M-box from the glycine decarboxylase P-subunit promoter in C2 Moricandia species

C2 photosynthesis operates by shuttling photorespiratory glycine (C2) from mesophyll (M) to bundle sheath (BS) cells, followed by decarboxylation and release of CO2 around RubisCO. C2 plants are characterized by low apparent photorespiration and enhanced refixation of photorespiratory CO2 and the C2 pathway is thought to represent an intermediate step for the evolution from C3 to C4 photosynthesis. Restriction of glycine decarboxylation to the BS cells is considered to be a prerequisite for C2 photosynthesis. In the C3 plant species Arabidopsis thaliana, a cis-element required for expression of the P-subunit of glycine decarboxylase (GDC—P) in M cells (termed the M-box) was previously identified in the promoter of A. thaliana glycine decarboxylase P-subunit 1 (AtGldp1). Consequently, the loss of this element restricted Gldp1 expression to the BS cells. To investigate conservation, Gldp promoter sequences from another C3 and two additional C2 Moricandia species were isolated by genome walking. In comparison to AtGldp1, the M-box was conserved in the promoter of C3 Moricandia moricandioides, but was not found in the promoters of M. nitens, M. suffruticosa, and M. arvensis, indicating the loss of the M-box from several C2 Moricandia species. The AtGldp1 M-box was further analyzed in detail using promoter::GUS fusions. Results show that interaction between two promoter regions containing predicted CAAT and GATA elements are required for expression of the GUS reporter in M cells and these elements including their spacing are conserved in the promoters of different members of the Brassicaceae