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. 2009 Jan;149(1):82–87. doi: 10.1104/pp.108.128553

Integrating Phylogeny into Studies of C4 Variation in the Grasses

Pascal-Antoine Christin 1,*, Nicolas Salamin 1, Elizabeth A Kellogg 1, Alberto Vicentini 1, Guillaume Besnard 1
PMCID: PMC2613744  PMID: 19126698

C4 photosynthesis consists of morphological and biochemical novelties that create a CO2 pump that concentrates CO2 around Rubisco (Kanai and Edwards, 1999), which decreases photorespiration and the resulting energy waste. Consequently, C4 photosynthesis provides a competitive advantage in all conditions where photorespiration costs become important, especially at high temperatures and in arid and saline conditions (Sage, 2001). Despite being used by only 3% of extant angiosperm species (Sage, 2004), C4 plants account for one-fifth of global terrestrial primary production (Ehleringer et al., 1997). This is mainly due to the high productivity of C4 monocots, especially C4 grasses, which are the most speciose C4 group (Sage, 2004). The C4 grasses dominate most open subtropical and tropical habitats, and some, such as maize (Zea mays), sorghum (Sorghum bicolor), millets (e.g. Pennisetum glaucum, Setaria italica), and sugarcane (Saccharum officinarum), are used as crops and have direct importance for human food consumption and/or as livestock fodder (Table I).

Table I.

Characteristics of the C4 grass lineages

No., Lineage number; n, number of C4 species. PCK, Phosphoenolpyruvate carboxykinase.

No.a Name Age Estimatesf n C3 Sister Group C4 Subtype(s) Cropsm Habitatn
1b Stipagrostis 15.1 (±4.6)–7.5 (±3.1) 50 Sartidiaa NADP-ME – Deserts and semideserts
NA
2b Aristida 28.8 (±5.2)–14.4 (±4.7) 290 Sartidiaa NADP-ME – Large ecological range
[44.4 (±7.5)–present]
3b Core Chloridoideae 32.0 (±4.4)–25.0 (±4.0) 1,410 Merxmuellera rangeiag NAD-ME and PCK Finger millet, teff Large ecological range
[37.6 (±6.6)–22.5 (±5.7)]
4b Centropodia 22.0 (±4.6)–11.3 (±5.5) 4 M. rangeiag NAD-ME – Dry open habitats (semideserts)
NA
5c Eriachne 11.5 (±3.6)–6.6 (±2.8) 40 Isachneagh NADP-ME – Warm open habitats (savannah)
NA
6b Arundinelleae 26.4 (±4.4)–7.9 (±3.4) 95 Centotheceae 2agh NADP-ME – Large ecological range
[31.7 (±5.9)–present]
7cd Panicum/Urochloa/Setaria clade 18.5 (±3.7)–16.4 (±3.6) >530 C3Neurachnea NADP-ME, NAD-ME, and PCK Foxtail, pearl, and proso millets Large ecological range
[15.9 (±3.7)–13.1 (±3.2)]
8c Neurachne munroi 4.4 (±3.3)–present 1 Neurachne tenuifoliaa NADP-ME – Dry open habitats (steppes)
NA
9c Echinochloa 13.8 (±3.5)–4.4 (±2.8) 30–40 Parodiophyllochloaai NADP-ME – Warm open habitats
[20.6 (±4.5)–2.6 (±1.3)]
10b Alloteropsis 15.3 (±3.5)–present 4–7 Forest shade cladeaj NADP-ME and PCK – Warm open habitats (savannah)
NA
11cd Digitaria 21.2 (±3.9)–8.1 (±3.4) 220 x = 9 Paniceaea NADP-ME Fonio Various warm open habitats
[15.9 (±3.7)–5.4 (±2)]
12b Andropogoneae 21.9 (±3.9)–17.1 (±4.1) 1,085 x = 10 Paniceaeak NADP-ME Maize, sorghum, sugarcane Large ecological range
[24.3 (±4.9)–19.1 (±4.5)]
13ab Paspalum clade 14.1 (±3.4)–8.5 (±3.1) >345 Streptostachys asperifoliaak NADP-ME Kodo millet Warm open habitats (savannah)
[11.7 (±3.1)–present]
13bc Ophiochloa clade 10.6 (±3.3)–2.8 (±1.9) 115 S. asperifoliaa NADP-ME – Large ecological range
[13.7 (±3.5)–4.4 (±2.1)]
14b Anthaenantiae 14.3 (±3.5)–present 1 Steinchisma cladeak NADP-ME – Warm open habitats (savannah)
[15 (±3.7)–present]
15c Streptostachys ramosa 15.5 (±3.5)–present 1 Cyphonanthusl NADP-ME – Warm open habitats (savannah)
[16.3 (±3.7)–present]
16b Panicum prionitis clade 10.4 (±2.9)–6.3 (±2.7) >5 Arthropogon lanceolatusak NADP-ME – Warm open habitats (savannah)
[11.2 (±2.9)–present]
17c Mesosetum clade 12.3 (±3.2)–11.3 (±3.0) 40 Homolepisak NADP-ME Warm open habitats (savannah)
[14.8 (±3.5)–13.9 (±3.4)]
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b

Independent origin confirmed by PEPC analyses (Christin et al., 2007).

c

Independent origin based on putative species relationships only.

d

Phylogeny from Vicentini et al. (2008) found Digitaria and the main x = 9 Paniceae C4 clade clustered together, suggesting a single C4 origin.

e

Previously named Leptocoryphium lanatum.

f

Christin et al. (2008) and Vicentini et al. (2008) into square brackets, ages are given in millions of years.

j

C3 subspecies of A. semialata could represent a reversion from C4 to C3 (Ibrahim et al., 2009).

m

Excluding fodders.

The biochemistry of the C4 pathway has been an active field of research over the last 40 years and is thus well described (Kanai and Edwards, 1999). However, many issues regarding C4 photosynthesis are still being investigated. A central problem has to do with the genetic regulation of C4 photosynthesis. The genetic mechanisms responsible for the transition from C3 to C4 remain poorly understood, despite extensive investigation on the part of numerous scientists (e.g. Covshoff et al., 2008; Lara et al., 2008). The evolution of the C4 pathway was previously thought to have involved relatively few key mutations (Ku et al., 1996), but recent studies showed that the C4 pathway of maize involves cell-specific expression for 18% of the genes (Sawers et al., 2007) and requires deep synchronization between mesophyll (M) and bundle sheath (BS) cells (Bailey et al., 2007). These transcriptional changes are likely to mediate, at least in part, the variation observed in BS and M plastid proteomes (Majeran et al., 2005, 2008). Rather than extensive changes in cis- and trans-acting regulatory elements, the segregation of enzymes between M and BS cells of C4 plants could have been acquired through changes in key regulatory elements changing M and BS cellular environments (Covshoff et al., 2008), leading to important differences in their transcriptomes (Sawers et al., 2007). In addition to the C4 enzymes, C4 photosynthesis evolution necessitated rearrangements of chloroplast envelope proteins (Bräutigam et al., 2008). Furthermore, transport of C4 intermediates between M and BS cells is probably not performed through simple diffusion, which suggests that other, unidentified, mechanisms exist (Sowinski et al., 2008), which may be yet another C4-specific adaptation.

Many of the enzymes that drive the carbon shuttle in C4 plants are also present in C3 plants but are involved in other aspects of plant growth and development (Monson, 2003). Tissue-specific regulation of C4 pathway enzymes appears to have been a crucial step in the evolution of C4 photosynthesis (Hibberd and Quick, 2002). One aspect of the pathway that remains poorly understood is the genetic components regulating the alteration of leaf anatomy (Kellogg, 1999). The developmental and genetic issues can be addressed with all C4 species, but the low number of model species used to date limits the generalization of the results.

Grasses have been the focus of much of the recent C4 research. For example, human-directed improvement of C3 grass crops, such as rice (Oryza sativa), barley (Hordeum vulgare), and wheat (Triticum aestivum), by introgression of C4 characteristics is receiving particular attention (Hibberd et al., 2008). Understanding the historical causes of C4 evolutionary and ecological success is another area of intense research activity (Cerling et al., 1997; Beerling and Osborne, 2006; Osborne and Beerling, 2006; Osborne, 2008). The ecological importance of grasses made this family a natural study system for investigating factors affecting the distribution and success of C4 plants (Taub, 2000; Carmo-Silva et al., 2007; Cabido et al., 2008; Edwards and Still, 2008). For instance, it has recently been shown that the oldest C4 origin in grasses is relatively young (approximately 30 million years old), and correlates with a marked decrease of atmospheric CO2 concentration (Christin et al., 2008; Vicentini et al., 2008). Since atmospheric CO2 concentration and air temperature both affect C4 plant success, the current changes in global climate will potentially trigger important perturbations in major ecosystems, and could affect the performance of extensively cultivated tropical cereals. Therefore, a complete understanding of C4 ecology and physiology is necessary for conservation biology and agriculture to face future climate changes (Sage and Kubien, 2003; Ainsworth et al., 2008).

Comparative analyses offer an attractive approach for both the study of genetic determinants of C4 photosynthesis (Christin et al., 2007) and the identification of attributes associated with it (Edwards et al., 2007; Edwards and Still, 2008). Such an approach requires comparing several independent origins of C4 plants to determine characteristics that are shared among them. Indeed, if two C4 species inherited the C4 trait from their common ancestor, they do not represent independent replicates. Ideally, comparative studies should consist of distinct C4 clades, known to represent distinct origins of the C4 pathway, as well as C3 sister groups to each of the C4 lineages. For this approach to work, species relationships have to be assessed by phylogenetic analyses, rendering the phylogenetic framework of systematic botany useful to evolutionary and physiological investigations.

C4 EVOLUTIONARY LINEAGES IN GRASSES

The grass family is composed of approximately 10,000 species, of which about 45% are C4 (Sage, 2004). Grass taxonomy recognizes between 12 and 13 main subfamilies but all C4 grasses belong to the PACMAD clade (Fig. 1; Duvall et al., 2007; or PACCMAD, Sánchez-Ken et al., 2007). Both the distribution of C4 grasses in distinct taxonomic groups and the high variability of their C4 syndrome led to the inference of multiple origins of the C4 pathway in this family (Sinha and Kellogg, 1996; Kellogg, 2001). Phylogenetic analyses of the subfamily Panicoideae further suggested that C4 photosynthesis appeared several times independently, although a single appearance followed by multiple reversions could not be excluded (Giussani et al., 2001; Duvall et al., 2003; Vicentini et al., 2008). The ancestral state reconstructions adopted in these studies are strongly dependent on species sampling and rely on statistical methods whose assumptions can produce different results. In addition, the transition rate from C3 to C4 could also change through time (Vicentini et al., 2008), for instance as a function of atmospheric CO2 levels (Christin et al., 2008) or after the acquisition of preadaptations to C4 photosynthesis (Sage, 2001). Finally, inferences of characters that affect the rates of speciation or extinction can yield erroneous conclusions if not carefully considered (Goldberg and Igić, 2008).

Figure 1.

Figure 1.

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Calibrated phylogenetic trees of the grass family. Phylogenetic trees are from independent studies by Christin et al. (2008; on the left; based on plastid markers) and Vicentini et al. (2008; on the right; based on one plastid and one nuclear marker). Branch lengths are proportional to elapsed time, in million years (Mya). All clades containing only C3 species are compressed (in black). Similarly, homogeneously C4 lineages are also compressed but in gray. C4 lineages represented by a single species are highlighted by a gray circle at the tip. C4 lineages are numbered according to Christin et al. (2008). Clade names and subfamilies are indicated between the two topologies. Asterisks indicate the position of the C3/C4 intermediate species S. hians. Mic, Micrairoideae; Chlor, Chloridoideae; Aris, Aristidoideae; PACMAD clade, subfamilies Panicoideae, Arundinoideae, Chloridoideae, Micrairoideae, Aristidoideae, and Danthonioideae. x = 9 and x = 10 Paniceae identify two distinct groups of this tribe that differ according to their basic chromosome number (9 and 10, respectively; Giussani et al., 2001).

Some studies have thus focused on the evolutionary dynamics of specific key enzymes involved in the C4 pathway, in particular phosphoenolpyruvate carboxylase (PEPC). The use of PEPC for the atmospheric CO2 fixation is one of the rare characteristics common to all C4 plants (Sinha and Kellogg, 1996; Sage, 2004), and its recruitment is an important step in the integration and optimization of C4 biochemistry (Svensson et al., 2003) and can be considered as a critical event in the evolution into a C4 plant. The presence of a Ser at position 780 of PEPC (numbered based on the maize sequence) is required for C4 function (Svensson et al., 2003) and was accompanied by many other recurrent adaptive amino acid changes (Christin et al., 2007) that left reliable C4-specific genetic signatures. Because changes along a DNA sequence are amenable to statistical modeling, they can easily be traced on a PEPC phylogenetic tree. This technique was used to identify the grass lineages that likely evolved the C4 trait independently (Table I; Christin et al., 2007, 2008).

C4 MODEL SPECIES IN GRASSES

The grasses contain few examples of closely related C3/C4 pairs, and those that exist are not easily accessible. Alloteropsis semialata contains a C3 and a C4 subspecies, which are closely related (Ibrahim et al., 2009) but differ in chromosome number (Liebenberg and Fossey, 2001) and so are presumably intersterile. A recent phylogenetic study suggested that C3 subspecies of A. semialata could represent an evolutionary reversion from C4 to C3 photosynthesis (Ibrahim et al., 2009). The genus Neurachne includes both C3 and C4 species (Moore and Edwards, 1989); these are native to Australia and grow in relatively inaccessible parts of the continent and have not, to our knowledge, been cultivated. The C3/C4 intermediate Steinchisma hians (formerly Panicum milioides) is sister to a group of C3 species, and has been crossed with them (Brown et al., 1985). Steinchisma as currently circumscribed is mainly South American.

Historically much of the work on C4 grasses focused on the genus Panicum because it appeared to have species with all possible photosynthetic pathways. Unfortunately, this genus was an assemblage of unrelated species (Aliscioni et al., 2003) whose taxonomy is being completely redefined (Morrone et al., 2007, 2008; Sede et al., 2008). The name Panicum should be restricted to a set of species that are all C4 with the subtype using the NAD-malic enzyme (NAD-ME), including switchgrass (Panicum virgatum). C3 species of Panicum are not closely related to true Panicum (Aliscioni et al., 2003).

Future C4 research should consider additional C4 species systems since including other independent lineages would increase the power of comparative analyses. In particular, Aristida and Stipagrostis, as well as the subfamily Chloridoideae, represent interesting C4 lineages. These groups are ecologically important (Table I) and strongly differ from the Panicoideae C4 species in terms of ecological attributes, such as aridity tolerance (Taub, 2000; Sato and Kubota, 2004; Carmo-Silva et al., 2007). They are species rich and widely distributed, facilitating sampling for more detailed study.

INTEGRATING PHYSIOLOGICAL STUDIES IN A PHYLOGENETIC CONTEXT

Understanding C4-specific growth, survival, and reproductive success, as well as the environmental conditions that influence these traits, is of prime ecological, agricultural, and evolutionary importance. Assessment of plant physiological traits, such as photosynthetic activity and efficiency, is time consuming, especially when performed under a range of environmental conditions. Therefore, physiological studies typically consider only a limited number of species. Unfortunately, due to the strong variations of the C4 pathway (Sinha and Kellogg, 1996), all C4 plants are far from being equivalent. Species sampling for physiological investigations is crucial to ensure the generalization of conclusions. As noted above, taxa that inherited their C4 trait from a common ancestor do not represent independent replicates. Their common ancestry can potentially lead to spurious correlations, which in turn can entangle characteristics due to the C4 trait and those resulting from a close phylogenetic relationship (Taub, 2000). A sound phylogenetic framework showed that a low carbonic anhydrase activity, previously attributed to C4 grasses (Gillon and Yakir, 2001), characterizes the whole PACMAD clade and is not linked to the C4 trait (Edwards et al., 2007). Thanks to its highly convergent nature, the C4 trait is present in numerous natural replicates. Species sampling for C4 physiological studies can take advantage of this by comparing species from independent C4 lineages, as well as each C4 clade with its C3 sister group (Table I). Therefore, species relationships deduced from molecular markers should serve as a guide for species sampling.

As a C4 study system, the grass family allows combining physiological, ecological, genomic, and evolutionary approaches, which are all necessary for a complete understanding of C4 photosynthesis. Integration of the wide knowledge we are gaining about C4 grasses to reach a full picture requires incorporation of evolutionary history by using phylogenetic information. Important efforts have led to a reasonably well-resolved phylogenetic tree for the grass family (e.g. Grass Phylogeny Working Group, 2001; Aliscioni et al., 2003; Duvall et al., 2007; Christin et al., 2008; Vicentini et al., 2008) but conflicts between plastid and nuclear markers (Fig. 1) still need to be resolved. Recent analyses of C4 genes have identified grass lineages that evolved the C4 pathway independently (Christin et al., 2007, 2008). These correspond to more than 15 independent replicates (Fig. 1), enabling wide-scale comparative studies to sort general attributes of C4 plants as well as particular ones. By taking advantage of the convergent nature of C4 photosynthesis, multidisciplinary studies in the grasses could bring a complete view of the selective pressures and genetic mechanisms responsible for the evolution of C4 photosynthesis and the factors that control the current distribution and success of C4 plants. C4 photosynthesis in grasses could become a model of macroevolution process when completely elucidated, from the selective pressures to the genetic mechanisms that led to its appearances.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Pascal-Antoine Christin (pascal-antoine.christin@unil.ch).

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