Molecular evolution of key metabolic genes during transitions to C<sub>4</sub> and <scp>CAM</scp> photosynthesis

Goolsby, Eric W.; Moore, Abigail J.; Hancock, Lillian P.; Vos, Jurriaan M. de; Edwards, Erika J.

doi:10.1002/ajb2.1051

Cited by 26 publications

(25 citation statements)

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“…C 4 photosynthesis especially has been well studied, perhaps due to the importance of C 4 grasses in agriculture, and we now understand a considerable amount about the evolutionary trajectory of the C 4 syndrome. The same cannot yet be said of CAM, although this is beginning to change (Silvera et al ., ; Horn et al ., ; Bone et al ., ; Heyduk et al ., ; Goolsby et al ., ; Males, ; Hancock et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

2019

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Summary Are evolutionary outcomes predictable? Adaptations that show repeated evolutionary convergence across the Tree of Life provide a special opportunity to dissect the context surrounding their origins, and identify any commonalities that may predict why certain traits evolved many times in particular clades and yet never evolved in others. The remarkable convergence of C4 and Crassulacean Acid Metabolism (CAM) photosynthesis in vascular plants makes them exceptional model systems for understanding the repeated evolution of complex phenotypes. This review highlights what we have learned about the recurring assembly of C4 and CAM, focusing on the increasingly predictable stepwise evolutionary integration of anatomy and biochemistry. With the caveat that we currently understand C4 evolution better than we do CAM, I propose a general model that explains and unites C4 and CAM evolutionary trajectories. Available data suggest that anatomical modifications are the ‘rate‐limiting step’ in each trajectory, which in large part determines the evolutionary accessibility of both syndromes. The idea that organismal structure exerts a primary influence on innovation is discussed in the context of other systems. Whether the rate‐limiting step occurs early or late in the evolutionary assembly of a new phenotype may have profound implications for its distribution across the Tree of Life.

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Section: Introductionmentioning

confidence: 99%

Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

2019

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“…Moreover, convergent evolution in several key amino acid residues of PEPC has been suggested to be associated with the origin of both C 4 and CAM (Christin et al 2007; Christin et al 2014; Goolsby et al 2018). A recent study has also confirmed the occurrence of multiple rounds of duplication within the major PEPC paralog (PEPC1E1) in the ancestral Portulacineae (Christin et al 2014).…”

Section: Resultsmentioning

confidence: 99%

Evolution of Portulacineae marked by gene tree conflict and gene family expansion associated with adaptation to harsh environments

Wang

Yang

Moore

et al. 2018

Preprint

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27Survival in harsh environments is associated with several adaptations in plants. Species in the 28 Portulacineae (Caryophyllales) have adapted to some of the most extreme terrestrial conditions on 29 Earth, including extreme heat, cold, and salinity. Here, we generated 52 new transcriptomes and 30 combined these with 30 previously generated transcriptomes, forming a dataset containing 68 species 31 of Portulacinaeae, seven from its sister clade Molluginaceae, and seven outgroups. We performed a 32 phylotranscriptomic analysis to examine patterns of molecular evolution within the Portulacineae. Our 33 inferred species tree topology was largely congruent with previous analyses. We also identified several 34 nodes that were characterized by excessive gene tree conflict and examined the potential influence of 35 outlying genes. We identified gene duplications throughout the Portulacineae, and found corroborating 36 evidence for previously identified paleopolyploidy events along with one newly identified event 37

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“…In our study, the CGS , HMT and MMT genes have been duplicated and diverged during evolution. In addition, previous research has also proposed that the evolution and divergence of metabolic pathways may be disclosed by comparing the sequence and the structure of genes of the same and different routes from organisms ( Fondi et al, 2007 ; Goolsby et al, 2018 ).Therefore, combining the evolutionary and expressional pattern of CGS , HMT and MMT genes, we proposed the evolutionary and functional models of Met biosynthetic pathway in plant lineages ( Fig. 6 ).…”

Section: Discussionmentioning

confidence: 99%

Molecular evolution and expression divergence of three key Met biosynthetic genes in plants:CGS,HMTandMMT

Zhao

Wang

Wei

et al. 2018

PeerJ

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Methionine (Met) is an essential sulfur-containing amino acid in animals. Cereal and legume crops with limiting levels of Met represent the major food and feed sources for animals. In plants, cystathionine gamma-synthase (CGS), methionine methyltransferase (MMT) and homocysteine methyltransferase (HMT) are committing enzymes synergistically synthesizing Met through the aspartate (Asp) family pathway and the S-methylmethionine (SMM) cycle. The biological functions of CGS, MMT and HMT genes have been respectively studied, whereas their evolution patterns and their contribution to the evolution of Met biosynthetic pathway in plants are unknown. In the present study, to reveal their evolution patterns and contribution, the evolutionary relationship of CGS, MMT and HMT gene families were reconstructed. The results showed that MMTs began in the ancestor of the land plants and kept conserved during evolution, while the CGSs and HMTs had diverged. The CGS genes were divided into two branches in the angiosperms, Class 1 and Class 2, of which Class 2 only contained the grasses. However, the HMT genes diverged into Class 1 and Class 2 in all of the seed plants. Further, the gene structure analysis revealed that the CGSs, MMTs and HMTs were relatively conserved except for the CGSs in Class 2. According to the expression of CGS, HMT and MMT genes in soybeans, as well as in the database of soybean, rice and Arabidopsis, the expression patterns of the MMTs were shown to be consistently higher in leaves than in seeds. However, the expression of CGSs and HMTs had diverged, either expressed higher in leaves or seeds, or showing fluctuated expression. Additionally, the functions of HMT genes had diverged into the repair of S-adenosylmethionine and SMM catabolism during the evolution. The results indicated that the CGS and HMT genes have experienced partial subfunctionalization. Finally, given the evolution and expression of the CGS, HMT and MMT gene families, we built the evolutionary model of the Met biosynthetic pathways in plants. The model proposed that the Asp family pathway existed in all the plant lineages, while the SMM cycle began in the ancestor of land plants and then began to diverge in the ancestor of seed plants. The model suggested that the evolution of Met biosynthetic pathway is basically consistent with that of plants, which might be vital to the growth and development of different botanical lineages during evolution.

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Molecular evolution of key metabolic genes during transitions to C₄ and CAM photosynthesis

Abstract: Our analyses reveal a new suite of amino acid residues putatively important for C and CAM function. We discuss both the advantages and challenges of using targeted enrichment sequence data for exploratory studies of molecular evolution.

Cited by 26 publications

References 72 publications

Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

Evolution of Portulacineae marked by gene tree conflict and gene family expansion associated with adaptation to harsh environments

Molecular evolution and expression divergence of three key Met biosynthetic genes in plants:CGS,HMTandMMT

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Molecular evolution of key metabolic genes during transitions to C4 and CAM photosynthesis

Abstract: Our analyses reveal a new suite of amino acid residues putatively important for C and CAM function. We discuss both the advantages and challenges of using targeted enrichment sequence data for exploratory studies of molecular evolution.

Cited by 26 publications

References 72 publications

Evolutionary trajectories, accessibility and other metaphors: the case of C4 and CAM photosynthesis

Evolutionary trajectories, accessibility and other metaphors: the case of C4 and CAM photosynthesis

Evolution of Portulacineae marked by gene tree conflict and gene family expansion associated with adaptation to harsh environments

Molecular evolution and expression divergence of three key Met biosynthetic genes in plants:CGS,HMTandMMT

Contact Info

Product

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Molecular evolution of key metabolic genes during transitions to C₄ and CAM photosynthesis

Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis

Evolutionary trajectories, accessibility and other metaphors: the case of C₄ and CAM photosynthesis