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765 I. 765 II. 767 III. 768 IV. 768 V. 770 VI. 771 VII. 773 VIII. 777 777 References 777 SUMMARY: C₄ photosynthesis is a physiological syndrome resulting from multiple anatomical and biochemical components, which function together to increase the CO₂ concentration around Rubisco and reduce photorespiration. It evolved independently multiple times and C₄ plants now dominate many biomes, especially in the tropics and subtropics. The C₄ syndrome comes in many flavours, with numerous phenotypic realizations of C₄ physiology and diverse ecological strategies. In this work, we analyse the events that happened in a C₃ context and enabled C₄ physiology in the descendants, those that generated the C₄ physiology, and those that happened in a C₄ background and opened novel ecological niches. Throughout the manuscript, we evaluate the biochemical and physiological evidence in a phylogenetic context, which demonstrates the importance of contingency in evolutionary trajectories and shows how these constrained the realized phenotype. We then discuss the physiological innovations that allowed C₄ plants to escape these constraints for two important dimensions of the ecological niche – growth rates and distribution along climatic gradients. This review shows that a comprehensive understanding of C₄ plant ecology can be achieved by accounting for evolutionary processes spread over millions of years, including the ancestral condition, functional convergence via independent evolutionary trajectories, and physiological diversification.

Plastid genomes have been widely used to infer phylogenetic relationships among plants, but the selective pressures driving their evolution have not been systematically investigated. In our study, we analyse all protein-coding plastid genes from 113 species of PACMAD grasses (Poaceae) to evaluate the selective pressures driving their evolution. Our analyses confirm that the gene encoding the large subunit of RubisCO (rbcL) evolved under strong positive selection after C₃–C₄ photosynthetic transitions. We highlight new codons in rbcL that underwent parallel changes, in particular those encoding the C-terminal part of the protein. C₃–C₄ photosynthetic shifts did not significantly affect the evolutionary dynamics of other plastid genes. Instead, while two-third of the plastid genes evolved under purifying selection or neutrality, 25 evolved under positive selection across the PAC-MAD clade. This set of genes encode for proteins involved in diverse functions, including self-replication of plastids and photosynthesis. Our results suggest that plastid genes widely adapt to changing ecological conditions, but factors driving this evolution largely remain to be identified.

The tree of life is resplendent with examples of convergent evolution, whereby distinct species evolve the same trait independently. Many highly convergent adaptations are also complex, which makes their repeated emergence surprising. In plants, the evolutionary history of two carbon concentrating mechanisms (CCMs) — C4 and crassulacean acid metabolism (CAM) photosynthesis — presents such a paradox. Both of these modifications of ancestral C3 photosynthesis require the integration of multiple anatomical and biochemical components, yet together they have evolved more than one hundred times. The presence of CCM enzymes in all plants suggests that a rudimentary CCM might emerge via relatively few genetic changes in potentiated lineages. Here, we propose that many of the complexities often associated with C4 and CAM photosynthesis may have evolved during a post-emergence optimization phase. The ongoing development of new model clades for young, emerging CCMs is enabling the comparative studies needed to test these ideas.Using the example of carbon concentrating mechanisms in plants, the authors of this Perspective provide evidence that broad comparative genomic analyses likely overestimate the genetic complexity underlying convergent evolution of complex traits.

Summary The origins of agriculture, 10 000 years ago, led to profound changes in the biology of plants exploited as grain crops, through the process of domestication. This special case of evolution under cultivation led to domesticated cereals and pulses requiring humans for their dispersal, but the accompanying mechanisms causing higher productivity in these plants remain unknown. The classical view of crop domestication is narrow, focusing on reproductive and seed traits including the dispersal, dormancy and size of seeds, without considering whole‐plant characteristics. However, the effects of initial domestication events can be inferred from consistent differences between traditional landraces and their wild progenitors. We studied how domestication increased the yields of Fertile Crescent cereals and pulses using a greenhouse experiment to compare landraces with wild progenitors. We grew eight crops: barley, einkorn and emmer wheat, oat, rye, chickpea, lentil and pea. In each case, comparison of multiple landraces with their wild progenitors enabled us to quantify the effects of domestication rather than subsequent crop diversification. To reveal the mechanisms underpinning domestication‐linked yield increases, we measured traits beyond those classically associated with domestication, including the rate and duration of growth, reproductive allocation, plant size and also seed mass and number. Cereal and pulse crops had on average 50% higher yields than their wild progenitors, resulting from a 40% greater final plant size, 90% greater individual seed mass and 38% less chaff or pod material, although this varied between species. Cereal crops also had a higher seed number per spike compared with their wild ancestors. However, there were no differences in growth rate, total seed number, proportion of reproductive biomass or the duration of growth. The domestication of Fertile Crescent crops resulted in larger seed size leading to a larger plant size, and also a reduction in chaff, with no decrease in seed number per individual, which proved a powerful package of traits for increasing yield. We propose that the important steps in the domestication process should be reconsidered, and the domestication syndrome broadened to include a wider range of traits. Lay Summary

• Lateral gene transfer (LGT) occurs in a broad range of prokaryotes and eukaryotes, occasionally promoting adaptation. LGT of functional nuclear genes has been reported among some plants, but systematic studies are needed to assess the frequency and facilitators of LGT. • We scanned the genomes of a diverse set of 17 grass species that span more than 50 Ma of divergence and include major crops to identify grass-to-grass protein-coding LGT. • We identified LGTs in 13 species, with significant variation in the amount each received. Rhizomatous species acquired statistically more genes, probably because this growth habit boosts opportunities for transfer into the germline. In addition, the amount of LGT increases with phylogenetic relatedness, which might reflect genomic compatibility among close relatives facilitating successful transfers. However, genetic exchanges among highly divergent species indicates that transfers can occur across almost the entire family. • Overall, we showed that LGT is a widespread phenomenon in grasses that has moved functional genes across the grass family into domesticated and wild species alike. Successful LGTs appear to increase with both opportunity and compatibility.

Societal Impact Statement Lateral gene transfer (LGT) refers to the transmission of genetic material without sexual reproduction. LGT is widespread in a number of plant species, including grasses. But how these genes of foreign origin got there is presently unknown. In this review, we show that transformation techniques used to genetically modify organisms could occur in the wild and be responsible for the frequently observed grass‐to‐grass LGTs. The distinction between natural evolutionary processes and genetic engineering might be arbitrary, and its validity will be further debated as agricultural biotechnology becomes more widely used and examples of “natural genetic engineering” through LGT increase. Summary Lateral gene transfer (LGT) is the transmission of genetic material among species without sexual reproduction. LGT was initially thought to be restricted to prokaryotes, but it has since been reported in a wide range of eukaryotes, including plants. Grasses seem to be particularly prone to LGT and frequently exchange genes among species. However, the mechanism(s) facilitating these transfers in this economically and ecologically important group of plants are debated. Here, we review vector‐mediated, direct tissue‐to‐tissue contact, wide‐crossing and reproductive contamination LGT mechanisms and discuss the likelihood of each in light of recent studies. Of particular relevance are transformation approaches that require minimal human intervention to transfer DNA among grasses in the lab that could mimic the mechanisms facilitating grass‐to‐grass LGT in the wild. These approaches include relatively simple techniques, such as pollen tube pathway‐mediated transformation, that take advantage of the permeability of the reproductive process to introduce alien genetic material from a third individual into an embryo. This process could be easily mirrored in the wild where pollen from one species lands on the stigma of another, acting as a source of alien DNA that can ultimately contaminate the reproductive process. This contamination is likely to be prevalent in wind pollinated species such as grasses, where the rates of illegitimate pollination will be high. In conclusion, plant transformation methods requiring minimal intervention are likely paralleled in the wild where they act as the mechanism underpinning LGT between distantly related grass species. La transferencia lateral de genes se refiere a la transmisión de material genético sin reproducción sexual. Se ha demostrado que la transferencia lateral de genes está muy extendida en varias especies de plantas, incluidas las gramíneas. Pero actualmente se desconoce cómo han llegado estos genes de origen foráneo. En esta revisión mostramos que las técnicas de transformación utilizadas para modificar genéticamente los organismos podrían ocurrir en la naturaleza y ser responsables de los LGT de gramínea a gramínea observados con frecuencia. La distinción entre los procesos evolutivos naturales y la ingeniería genética podría ser arbitraria, y su validez se seguirá debatiendo a medida que la biotecnología agrícola se generalice y aumenten los ejemplos de “ingeniería genética natural” mediante transferencia lateral de genes. Le transfert latéral de gènes désigne la transmission de matériel génétique sans reproduction sexuée. Il a été démontré que le transfert latéral de gènes est très répandu chez certaines plantes, y compris les graminées. On ignore actuellement comment ces gènes d'origine étrangère sont passés d'une espèce à l'autre. Dans cette revue, nous montrons que les techniques de transformation utilisées pour modifier génétiquement des organismes pourraient se produire dans la nature et être à l'origine des transferts latéraux de gènes entre graminées fréquemment observés. La distinction entre les processus évolutifs naturels et le génie génétique pourrait donc être vue comme arbitraire. La validité de cette distinction est susceptible d'être de plus en plus débattue au fur et à mesure que la biotechnologie agricole se répand et que les exemples de “génie génétique naturel” par transfert latéral de gènes se multiplient. Lateral gene transfer (LGT) refers to the transmission of genetic material without sexual reproduction. LGT is widespread in a number of plant species, including grasses. But how these genes of foreign origin got there is presently unknown. In this review, we show that transformation techniques used to genetically modify organisms could occur in the wild and be responsible for the frequently observed grass‐to‐grass LGTs. The distinction between natural evolutionary processes and genetic engineering might be arbitrary, and its validity will be further debated as agricultural biotechnology becomes more widely used and examples of “natural genetic engineering” through LGT increase.

Tropical grasses fuel the majority of fires on Earth. In fire‐prone landscapes, enhanced flammability may be adaptive for grasses via the maintenance of an open canopy and an increase in spatiotemporal opportunities for recruitment and regeneration. In addition, by burning intensely but briefly, high flammability may protect resprouting buds from lethal temperatures. Despite these potential benefits of high flammability to fire‐prone grasses, variation in flammability among grass species, and how trait differences underpin this variation, remains unknown. By burning leaves and plant parts, we experimentally determined how five plant traits (biomass quantity, biomass density, biomass moisture content, leaf surface‐area‐to‐volume ratio and leaf effective heat of combustion) combined to determine the three components of flammability (ignitability, sustainability and combustibility) at the leaf and plant scales in 25 grass species of fire‐prone South African grasslands at a time of peak fire occurrence. The influence of evolutionary history on flammability was assessed based on a phylogeny built here for the study species. Grass species differed significantly in all components of flammability. Accounting for evolutionary history helped to explain patterns in leaf‐scale combustibility and sustainability. The five measured plant traits predicted components of flammability, particularly leaf ignitability and plant combustibility in which 70% and 58% of variation, respectively, could be explained by a combination of the traits. Total above‐ground biomass was a key driver of combustibility and sustainability with high biomass species burning more intensely and for longer, and producing the highest predicted fire spread rates. Moisture content was the main influence on ignitability, where species with higher moisture contents took longer to ignite and once alight burnt at a slower rate. Biomass density, leaf surface‐area‐to‐volume ratio and leaf effective heat of combustion were weaker predictors of flammability components. Synthesis. We demonstrate that grass flammability is predicted from easily measurable plant functional traits and is influenced by evolutionary history with some components showing phylogenetic signal. Grasses are not homogenous fuels to fire. Rather, species differ in functional traits that in turn demonstrably influence flammability. This diversity is consistent with the idea that flammability may be an adaptive trait for grasses of fire‐prone ecosystems.

A well-known case of evolutionary adaptation is that of ribulose-1,5-bisphosphate carboxylase (RubisCO), the enzyme responsible for fixation of CO ₂ during photosynthesis. Although the majority of plants use the ancestral C ₃ photosynthetic pathway, many flowering plants have evolved a derived pathway named C ₄ photosynthesis. The latter concentrates CO ₂, and C ₄ RubisCOs consequently have lower specificity for, and faster turnover of, CO ₂. The C ₄ forms result from convergent evolution in multiple clades, with substitutions at a small number of sites under positive selection. To understand the physical constraints on these evolutionary changes, we reconstructed in silico ancestral sequences and 3D structures of RubisCO from a large group of related C ₃ and C ₄ species. We were able to precisely track their past evolutionary trajectories, identify mutations on each branch of the phylogeny, and evaluate their stability effect. We show that RubisCO evolution has been constrained by stability-activity tradeoffs similar in character to those previously identified in laboratory-based experiments. The C ₄ properties require a subset of several ancestral destabilizing mutations, which from their location in the structure are inferred to mainly be involved in enhancing conformational flexibility of the open-closed transition in the catalytic cycle. These mutations are near, but not in, the active site or at intersubunit interfaces. The C ₃ to C ₄ transition is preceded by a sustained period in which stability of the enzyme is increased, creating the capacity to accept the functionally necessary destabilizing mutations, and is immediately followed by compensatory mutations that restore global stability.

The cacti are one of the most celebrated radiations of succulent plants. There has been much speculation about their age, but progress in dating cactus origins has been hindered by the lack of fossil data for cacti or their close relatives. Using a hybrid phylogenomic approach, we estimated that the cactus lineage diverged from its closest relatives [almost equal to]35 million years ago (Ma). However, major diversification events in cacti were more recent, with most species-rich clades originating in the late Miocene, [almost equal to]10-5 Ma. Diversification rates of several cactus lineages rival other estimates of extremely rapid speciation in plants. Major cactus radiations were contemporaneous with those of South African ice plants and North American agaves, revealing a simultaneous diversification of several of the world's major succulent plant lineages across multiple continents. This short geological time period also harbored the majority of origins of C₄ photosynthesis and the global rise of C₄ grasslands. A global expansion of arid environments during this time could have provided new ecological opportunity for both succulent and C₄ plant syndromes. Alternatively, recent work has identified a substantial decline in atmospheric CO₂ [almost equal to]15-8 Ma, which would have strongly favored C₄ evolution and expansion of C₄-dominated grasslands. Lowered atmospheric CO₂ would also substantially exacerbate plant water stress in marginally arid environments, providing preadapted succulent plants with a sharp advantage in a broader set of ecological conditions and promoting their rapid diversification across the landscape.