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Plant Mol Biol (2016) 91:193–209 DOI 10.1007/s11103-016-0455-x Transcriptome comparisons shed light on the pre-condition and potential barrier for C4 photosynthesis evolution in eudicots 1 1 1 Yimin Tao • Ming-Ju Amy Lyu • Xin-Guang Zhu Received: 18 August 2015 / Accepted: 14 February 2016 / Published online: 18 February 2016 Ó Springer Science+Business Media Dordrecht 2016 Abstract C4 photosynthesis evolved independently from Keywords C4 photosynthesis Á C4 evolution Á C3 photosynthesis in more than 60 lineages. Most of the C4 Transcriptome Á Flaveria Á PPT Á Stress lineages are clustered together in the order Poales and the order Caryophyllales while many other angiosperm orders do not have C4 species, suggesting the existence of bio- Introduction logical pre-conditions in the ancestral C3 species that facilitate the evolution of C4 photosynthesis in these lin- C4 photosynthesis has evolved independently from C3 eages. To explore pre-adaptations for C4 photosynthesis photosynthesis in at least 62 lineages, including 36 lineages evolution, we classified C4 lineages into the C4-poor and in the eudicots, 18 lineages in the grass family and 6 lin- the C4-rich groups based on the percentage of C4 species in eages in the sedge family (Sage et al. 2011). Most of C4 different genera and conducted a comprehensive compar- lineages are clustered together in the order Poales and the ison on the transcriptomic changes between the non-C4 order Caryophyllales while many other angiosperm orders species from the C4-poor and the C4-rich groups. Results do not have any C4 species. This biased distribution of C4 show that species in the C4-rich group showed higher species suggests that few plant groups possess appropriate expression of genes related to oxidoreductase activity, light sets of environmental, metabolic, and anatomical condi- reaction components, terpene synthesis, secondary cell tions that favor the evolution of C4 photosynthesis (Sage synthesis, C4 cycle related genes and genes related to 2001). nucleotide metabolism and senescence. In contrast, C4- Many environmental conditions that promote C4 evo- poor group showed up-regulation of a PEP/Pi translocator, lution have been proposed, such as the decline of atmo- genes related to signaling pathway, stress response, defense spheric CO2 concentration (Christin et al. 2008), high light, response and plant hormone metabolism (ethylene and warm temperature, increasing aridity (Sage 2001), wild fire brassinosteroid). The implications of these transcriptomic (Osborne and Beerling 2006), migration into open canopy differences between the C4-rich and C4-poor groups to C4 system (Osborne and Freckleton 2009) and reduction of evolution are discussed. mean annual precipitation (Edwards and Smith 2010). Some biological pre-conditions in non-C4 state that pro- Electronic supplementary material The online version of this mote C4 evolution have also been proposed. Some article (doi:10.1007/s11103-016-0455-x) contains supplementary anatomical or biochemical features that were gained in the material, which is available to authorized users. ancestral non-C4 background can facilitate the transition from C photosynthesis to C photosynthesis (Sage 2001). & Xin-Guang Zhu 3 4 [email protected] For example, large bundle sheath cells in the PACMAD clade of grasses could increase the probability of C4 evo- 1 CAS-Key Laboratory for Computational Biology and State lution in this clade (Christin et al. 2013; Griffiths et al. Key Laboratory for Hybrid Rice, Partner Institute for 2013). Besides, traits of salt tolerance were found to be Computational Biology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, present significantly more frequently in C4 grass lineages China compared to their C3 counterparts (Bromham and Bennett 123 194 Plant Mol Biol (2016) 91:193–209 2014). Detailed comparative studies in Flaveria genus respectively (Edwards and Ku 1987; McKown et al. 2005). suggested that the re-localization of glycine decarboxylase Clade B and clade A belong to two independent lineages of (GDC) into the bundle sheath cell and re-fixation of pho- C4 photosynthesis evolution in the genus Flaveria (Sage torespired CO2 (termed C2 photosynthesis) have evolved et al. 2011). Based on the reconstructed phylogenetic tree, before the emergence of C4 metabolic cycle and may also clade A of Flaveria genus contains 4 C3–C4 intermediate have facilitated the subsequent evolution of C4 photosyn- species and 4 C4 species (McKown et al. 2005). Hence the thesis (Sage et al. 2012). Theoretical studies using con- clade A was classified as the C4-rich group (C50 % C4 straint-based model on metabolic networks of the Flaveria abundance). However, Clade B of Flaveria genus contains species further showed that the evolution of C2 photosyn- 8C3–C4 intermediate species and 1 C4-like species but no thesis created an unbalanced nitrogen metabolism between true C4 species (McKown et al. 2005). Though the clade B bundle sheath and mesophyll cells, which could be rescued has no true C4 species identified so far, Flaveria brownii, by the recruitment of some enzymes that were later used as the C4-like species in the clade B, already has a complete components in C4 photosynthesis (Mallmann et al. 2014). C4 photosynthetic pathway, as shown by its gene expres- Recently, John et al. (2014) showed that the ratio of sion profile, gas exchange property and resource use effi- expression abundance between bundle sheath and mesophyll ciency (Monson et al. 1987; Sage et al. 2011). Therefore cells for the genes encoding core C4 enzymes are highly the clade B of Flaveria genus is an independent C4 evo- convergent in different C4 lineages, such as Zea mays, Sor- lutionary emergence (Sage et al. 2011) and was classified ghum bicolor, and Setaria viridis (John et al. 2014). Fur- as a C4-poor group in this study. RNA-seq data of F. thermore, using a deep evolutionary comparison, Aubry et al. anomala and F. ramosissima were retrieved from published (2014) showed that parallel recruitment of homologous dataset with four replicates for each species (Mallmann transcription factors for induction of C4 photosynthesis and et al. 2014). maintenance of cell specific expression patterns in two To discover more general pre-conditions towards C4 independent origins of C4 photosynthesis whose last com- photosynthesis, all eudicot species in the 1KP data set mon ancestor diverged *140 million years ago (Aubry et al. (http://www.oneKP.com/samples/list.php) were screened 2014). Furthermore, though there are metabolic variations of for sampling. All genera with the existence of C4 species C4 photosynthesis, C4 photosynthesis uses similar core were selected for C4 abundance calculation. The total enzymes for the C4 shuttle. All these raise a possibility that number of species was decided based on the estimation of there might be conserved metabolic and regulatory features The Plant List (http://www.theplantlist.org) and C4 species in the ancestors of C4 species, which facilitate the evolution number were collected from literature (Sage et al. 2011) of C4 photosynthesis from C3 ancestors. In this study, we and summarized in the Table 4. Finally, 12 eudicot C3 study this question by comparing transcriptomics profiles of species from 8 genera were identified (Table 5). RNA-seq species in genera with different C4 species abundance, i.e. data of mature leaf tissue for these 12 species (one replicate the ratio of the number of known C4 species to the total for each species) were downloaded from web data source number of species in a genera. By such a comparison, we (http://web.corral.tacc.utexas.edu/OneKP/). assume that (a) extant C3 species in these contrasting groups still reserve regulatory and metabolic features which have Minimal protein coding gene set for Arabidopsis conferred different probabilities of evolving C4 photosyn- thaliana genome thesis; (b) these different regulatory and metabolic features can be reflected in the transcriptomics data. Transcriptomics The 12 species analyzed were widely distributed in eudi- features presented in the C4-rich group but not in the C4-poor cots. Genome information is available for none of them. As group are inferred as potential pre-conditions for C4 photo- a result, the genome of Arabidopsis thaliana (A. thaliana), synthesis evolution. Features of the transcriptomic profile a representative eudicot model plant, was chosen as ref- presented in the C4-poor group but not in the C4-rich group erence for reads mapping. are potential metabolic or regulatory barriers that decrease The genome of A. thaliana experienced two whole the possibility of C4 photosynthesis evolution. genome duplication (WGD) events (WGDa and WGDb) recently (Bowers et al. 2003; Vision et al. 2000), which happened specifically within the cruifer (Brassicaceae) Materials and methods lineage (Tang et al. 2008). Considering the existence of these two WGD events and other lineage-specific gene Taxon sampling and C4 abundance determination duplications, the minimal genome of A. thaliana was pro- posed and constructed for gene expression quantification Flaveria anomala and Flaveria ramosissima are C3–C4 across species (Brautigam et al. 2011). In our study, we intermediate species basal to clade B and clade A adopted this minimal protein coding gene set (Brautigam 123 Plant Mol Biol (2016) 91:193–209 195 et al. 2011) and updated it with TAIR10 release (Online expressed in 12 species were identified and used for fol- Resource S4). Compared to the TAIR9, there are 79 new lowing analyses. protein-coding genes added and 42 protein-coding genes removed in the TAIR10 release. For these 79 newly added Identification of the differentially expressed genes genes into TAIR10, homologous search was conducted and significantly changed pathways between against peptide sequences of all protein-coding genes in the C4-rich and C4-poor groups TAIR10 using blastp to identify potential gene duplication events (Camacho et al. 2009). Based on the alignment Procedures for identification of differentially expressed identity, 8 of these 79 protein-coding genes were identified genes and significantly changed pathways between the C4- to be duplicated.

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