Triticeae is a plant family in the Poaceae of Gramineae which includes many domesticated species. The main crops found in this family include wheat (see taxonomy of wheat), barley, and rye. Other crop species include some used for human consumption and others for animal feed or pasture conservation. The Triticeae contains 33 genera, of which the main cultivated or edible species come from seven genera: Aegilops, Amblyopyrum, Elymus, Hordeum, Leymus, Secale, and Triticum.

Among the cultivated species in the world, this tribe has some of the most complex genetic histories. Due to the large number of species and complex origins of Triticeae plants, natural hybridization events between different species and genera are relatively common. Bread wheat is an example, as it contains genomes from three different wheat species, with only one genome coming from a plant in the Triticum genus.

Triticeae species are widely distributed around the world, with the main concentration in the temperate and Mediterranean regions of the northern hemisphere. They can be found in Eurasia, North and South America, Australia, and Northern Africa (Guo and Guo, 1991, Acta Botanica Boreali-Occidentalia Sinica, (2): 159-169). The ecological environments of Triticeae plants are also extremely diverse, ranging from forest edges, shrubs, swamps, grasslands, valleys, deserts, and steppes in natural state, to mountainou areas and farmland developed by humans. Triticeae species can be found from coastal areas to the Qinghai-Tibet Plateau at an altitude of over 4 000 meters (Lu and Liu, 1992, Bulletin of Botany, 9(1): 26-31; Lu, 1995, Biodiversity Science, 3(2): 63-68; Li et al., 2019). The diversity of environmental adaptation of Triticeae species plays an extremely important role in the improvement of cereal crops.

1 Genetic Improvement

Triticeae plants not only include important grain crops closely related to human life, such as barley, wheat, rye, and the artificial hybrid Triticale, but also many forage species with important economic value, such as Laomangmai (Elymus sibiricus L.), Bingcao (Agropyron cristatum (L.) Gaertn.), and Xinmaicao (Psathyrostachys juncea (Fisch.) Nevski).

In addition, some perennial Triticeae species, such as Shashenglaicao (Leymus arenarius (L.) Hochst), Dalaicao (Leymus racemosus (L.) Tzvel), and Yanmaicao (Elytrigia repens (L.) Nevski) have well-developed underground stems and strong drought tolerance, making them valuable for soil and water conservation and windbreaks (Pratap et al., 2005). Most Triticeae plants contain abundant genes for large spikes, resistance to pests, diseases, drought, cold, and salt, forming a huge and diverse genetic pool provides a good genetic background for the improvement of wheat crops and the improvement of forage quality. It plays an important role in the rational development and utilization of grasslands, the maintenance of grassland ecosystem balance, and soil and water conservation (Crane and Carman, 1987; Asay, 1992).

Currently, there are many examples of using beneficial genes from wild relatives of Triticeae to improve wheat varieties. For instance, genes for resistance to stripe rust, powdery mildew, and insect pests have been transferred from Elytrigia intermedia (Host) Nevski, Elytrigia elongata (Host) Nevski, Aegilops speltoides Tausch, and rye to common wheat (Sharma and Gill, 1983; Friebe et al., 1990; Lutz et al., 1995). For such a huge and economically important genetic pool of the Triticeae, it is necessary to conduct in-depth research to gain a comprehensive understanding of the systematics and evolutionary history of the Triticeae, and also to better apply Triticeae plant resources to the genetic improvement of cereal and forage crops.

2 Origin and Divergence Time of Triticeae

In evolutionary biology research, estimating divergence time between species is of great significance. The determination of species divergence time is a prerequisite and basis for studying evolutionary events such as speciation, origin, and distribution. Fossil evidence is the primary evidence for the origin time of species, but the lack of fossil evidence for many taxa makes it difficult to determine their origin time. The molecular clock method is not limited by the lack of fossil evidence and is a powerful supplement to determining  origin time of species, so it has been widely used in various taxa (Sanderson and Doyle, 2001).

Currently, with the rapid development of molecular biology techniques, estimating species divergence time using DNA sequences has become an important research method. For example, Bremer et al. (2000) speculated that the main groups of existing Monocotyledon began to differentiate 100 million years ago by using single genes. Cronn et al. (2002) showed that the cultivated cotton began to differentiate from its wild ancestors between. 1.2~6.08 million years ago.

Three main methods are currently used to estimate the divergence time between species: global molecular clocks, local molecular clocks, and relaxed molecular clocks. As early as 1965, Zuckerkandl and Pauling (1965) proposed the global molecular clock hypothesis, which assumes that the molecular rate is constant. The divergence times of all nodes in the evolutionary tree can be estimated by calibrating one fossil point, and geological time is then converted using the geological age information of each node on the evolutionary tree and the branch length between each sequence.

However, the assumption of a global molecular clock is not ideal due to differences in nucleotide substitution rates (Rutschmann, 2006). The second method is the local molecular clock, which is a non-parametric rate smoothing algorithm (NPRS) based on a local molecular clock model for estimating the divergence time of taxa (Sanderson, 1997). This algorithm combines likelihood and non-parametric methods used in NPRS and can be calibrated with multiple fossil points while maintaining some flexibility and superiority. The third method is the relaxed molecular clock, which considers the different possibilities of molecular clocks between different taxa and different historical periods. The relaxed molecular clock model uses a multi-parameter model to calculate the change in evolutionary rate over time and uses MCMC algorithm to infer the posterior probability of divergence rate and time (Drummond et al., 2006). Its another notable feature is that it does not require a specific topology for the initial phylogenetic tree, considering the uncertainty of the phylogenetic tree, and can more accurately estimate species divergence time. Currently, it has been found that few taxa conform to the ideal state of molecular clocks. Therefore, the relaxed molecular clock method is mainly used to estimate species divergence time.

The research of molecular evolution has been developed rapidly with the discovery of Molecular clock and the proposition of neutral principle (Kimura, 1968). Inferences about the origin and divergence times of taxa are based on the specific phylogenetic relationships of the taxa, geological and paleontological fossil evidence. So far, many important angiosperm fossils have been discovered, so the estimation of the origin and divergence time of angiosperms increasingly reliable which can more accurately infer the origin time, location, and discontinuous divergence of many taxa (Crepet et al., 2004).

Therefore, the divergence time of the Poaceae can also be estimated using fossil records. so far, there are relatively few fossil records have been found, especially in the Cretaceous and early Paleogene. Apart from limited pollen records in the early Paleogene, there are no more fossil records (Crepet and Feldman, 1991). Linder (1998) believed that the Poaceae originated in the Upper Cretaceous. Jacobs et al. (1999) found reliable pollen fossils of Poaceae in the Paleocene strata of South America and Africa, dating back to about 55~60 million years ago. Pollen fossils possibly belonging to Poaceae or its close relatives were also found in the Maastrichtian strata of Africa and South America, dating back to around 70 million years ago (Kellogg, 2001).

So far, a series of macrofossils of the Poaceae have been discovered so far. The earliest recognized Poaceae fossil was a spikelet found in the Oligocene strata of eastern Missouri, USA, dating back to about 23~36 million years ago, which is the first macrofossil record of the Poaceae (Thomasson, 1988). However, the oldest typical Poaceae fossil was found in the Paleogene-Eocene boundary strata in western Tennessee, USA, dating back to about 55 million years ago, including a series of fossils of spikelets, leaves, inflorescences, and two complete plants.

Kellogg (2001) believed that the ancestor of Poaceae may have originated from 70 to 55 million years ago based on direct fossil evidence. However, Prasad (2005) found that early Poaceae fossils already existed in dinosaur feces in the late Cretaceous, and he believed that the core Poaceae had begun to originate and differentiate 65 million years ago, this relatively reliable fossil evidence indicates that Poaceae already existed between the Paleogene and Eocene. Using the above fossil evidence, Liu (2014) used the relaxed molecular clock method to infer that the origin and diversification of the Triticeae tribe occurred in the early Miocene of the Tertiary period.

3 Evolution of the Triticeae

The Triticeae and its sister tribe Bromeae (possible cultivated species: Bromus mango S. America) form a sister evolutionary branch with Poeae and Aveneae (Oats). Gene flow among these groups was a characteristic of early stages of their evolution. For example, Poeae and Aveneae share the same genetic markers with barley and the other ten members of the Triticeae, while Bromeae carries the same wheat markers as 19 genera of the Triticeae (Kubo et al., 2005). The genera in the Triticeae include diploid, allotetraploid, and/or allohexaploid genomes, with varying abilities to form allopolyploid genomes within the tribe. Among the tribe, most diploid species are closely related to Aegilops, and there are many distal members (earliest branching points), including Hordeum, Eremian, and Psathyrostachys.

Many genera and species in Triticeae are allopolyploids, with more chromosomes than typical diploids. The determination of genome symbols provides great convenience for recognizing the number and boundaries of diploid and polyploid genera in the Triticeae (Table 1). Typical allopolyploids are tetraploids or hexaploids, XXYY or XXYYZZ. The production of polyploid species is due to natural and random events that polyploid plants can tolerate. Natural allopolyploid plants have selective advantages, and some may allow recombination of distant genetic material. Poulard wheat, as a stable allotetraploid wheat, is one example.

Table 1 Genomes of some Triticeae genera and species

One of the earliest branches in Triticeae, Pseudoroegeneria, is an allopolyploid consisting of the genomes StSt from one branch and the genome HH from another branch, which can be found in Elymus (HHStSt) (Mason-Gamer, 2004), but this may also be due to gene introgression from Australian and Agropyron wheatgrass (Liu et al., 2006). Elymus mainly contains Pseudoroegeneria mtDNA (Mason-Gamer et al., 2002).

Rye (cultivated rye) may be a very early branch of goatgrass (or goatgrass may be an early branch of rye grass), as these branches are almost contemporaneous with the branch between diploid wheat and Aegilops tauschii. Studies in Anatolia now indicate that rye (Secale) was cultivated before the Holocene, but not domesticated, which also provides evidence for the cultivation of wheat. As the climate changed, the cultivation of Secale decreased, and at the same time, other barley and wheat varieties may have been cultivated, but humans have hardly changed them.

4 Utilization of the Triticeae

The utilization of the Triticeae can be traced back to 23 000 years ago in the eastern Mediterranean region, where wild Triticeae were extensively used (Weiss et al., 2004). Evidence of Triticeae grain processing and cooking was also found in Ohala II (Israel) (Piperno et al., 2004). Many Triticeae varieties in the upper Fertile Crescent, Levant, and central Anatolia regions seem to have been domesticated (Lev-Yadun et al., 2000; Weiss et al., 2006).

There is also research indicating that wheat cultivation may be related to grazing,, and some scholars trace it back to the Neolithic period, known as the Garden Hunting Hypothesis. In this hypothesis, In this hypothesis, residents attract wildlife by planting or sharing grains, so that their livestock can be hunted and killed near the settlement.. Today, rye and other wheat varieties are used as feed for grazing animals, especially cows.

In addition, Triticeae are closely related to human health, as gluten (storage protein) in Triticeae is associated with gluten-sensitive diseases. Although oats were once thought to have similar potential, recent research suggests that oat gluten sensitivity is the result of contamination. Wheat gluten research is very important for determining the relationship between gluten and gastrointestinal, allergic, and autoimmune diseases (Silano et al., 2007). According to recent biochemical and immunological studies of proteins, their evolution is to prevent mammals from specializing or persistently feeding on their seeds (Shan et al., 2005; Mamone et al., 2007). A recent publication has even raised doubts about the safety of wheat consumption (Bernardo et al., 2007). The overlapping properties of food preparation make these proteins more useful than single cereal cultivars, and there is evidence that variable tolerance to wheat gluten reflects early childhood environment and genetic qualities (Zubillaga et al., 2002; Collin et al., 2007; Guandalini, 2007).

Authors’ contribution

LJH was responsible for the literature collection and writing of the paper; ZJ was the project leader and was responsible for revising and finalizing the paper; WZR was responsible for paper translation; DDY was responsible for revision and proofreading. All authors read and approved the final manuscript.

Acknowledgements

This study was supported by Funding for Cuixi Innovation Research & Development Project of Cuixi Academy of Biotechnology, Zhuji.

References

Asay K.H., 1992, Breeding potentials in perennial Triticeae grasses, Hereditas, 116(1‐2): 167-173.

https://doi.org/10.1111/j.1601-5223.1992.tb00223.x

Backlund M., Oxelman B., and Bremer B., 2000, Phylogenetic relationships within the Gentianales based on ndhF and rbcL sequences, with particular reference to the Loganiaceae, American Journal of Botany, 87(7): 1029-1043.

https://doi.org/10.2307/2657003

Bernardo D., Garrote J.A., Fernández-Salazar L., Riestra S., and Arranz E., 2007, Is gliadin really safe for non-coeliac individuals? Production of interleukin 15 in biopsy culture from non-coeliac individuals challenged with gliadin peptides, Gut, 56(6): 889-890.

https://doi.org/10.1136/gut.2006.118265

Collin P., Mäki M., and Kaukinen K., 2007, Safe gluten threshold for patients with celiac disease: some patients are more tolerant than others, Am. J. Clin. Nutr., 86(1): 260-260.

https://doi.org/10.1093/ajcn/86.1.260

Crane C.F., and Carman J.G., 1987, Mechanisms of apomixis in Elymus rectisetus from eastern Australia and New Zealand, American journal of botany, 74(4): 477-496.

https://doi.org/10.1002/j.1537-2197.1987.tb08668.x

Crepet W.L., and Feldman G.D., 1991, The earliest remains of grasses in the fossil record, American Journal of Botany, 78(7): 1010-1014.

https://doi.org/10.1002/j.1537-2197.1991.tb14506.x

Crepet W.L., Nixon K.C., and Gandolfo M.A., 2004, Fossil evidence and phylogeny: the age of major angiosperm clades based on mesofossil and macrofossil evidence from Cretaceous deposits, American Journal of Botany, 91(10): 1666-1682.

https://doi.org/10.3732/ajb.91.10.1666

Cronn R., Cedroni M., Haselkorn T., Grover C., and Wendel J.F., 2002, PCR-mediated recombination in amplification products derived from polyploid cotton, Theoretical and Applied Genetics, 104(2-3): 482-489.

https://doi.org/10.1007/s001220100741

Drummond A.J., Ho S.Y., Phillips M.J., and Rambaut A., 2006, Relaxed phylogenetics and dating with confidence, PLoS biology, 4(5): e88.

https://doi.org/10.1371/journal.pbio.0040088

Friebe B., Hatchett J.H., Sears R.G., and Gill B.S., 1990, Transfer of Hessian fly resistance from 'Chaupon'rye to hexaploid wheat via a 2BS/2RL wheat-rye chromosome translocation, Theoretical and applied genetics, 79(3): 385-389.

https://doi.org/10.1007/BF01186083

Guandalini S., 2007, The influence of gluten: weaning recommendations for healthy children and children at risk for celiac disease. Nestlé Nutrition Workshop Series. Paediatric Programme, Nestlé Nutrition Workshop Series: Pediatric Program, 60. pp. 139-155.

https://doi.org/10.1159/000106366

Jacobs B.F., and Jacobs K.L.L., 1999, The origin of grass-dominated ecosystems, Annals of the Missouri Botanical Garden, 86(2): 590-643.

https://doi.org/10.2307/2666186

Kellogg E. A., 2001, Evolutionary history of the grasses, Plant physiology, 125(3): 1198-1205.

https://doi.org/10.1104/pp.125.3.1198

Kimura M., 1968, Evolutionary rate at the molecular level, Nature, 217(5129): 624-626.

https://doi.org/10.1038/217624a0

Kubo N., Salomon B., Komatsuda T., von Bothmer R., and Kadowaki K., 2005, Structural and distributional variation of mitochondrial rps2 genes in the tribe Triticeae (Poaceae), Theor Appl Genet., 110 (6): 995-1002.

https://doi.org/10.1007/s00122-004-1839-x

Lev-Yadun S., Gopher A., and Abbo S., 2000, (ARCHAEOLOGY:Enhanced:) The Cradle of Agriculture, Science, 288 (5471): 1602-1603.

https://doi.org/10.1126/science.288.5471.1602

Li J.H., Qi T.Y., and Fang X.J., 2019, Qingke, a Plateau Barley Feeds Tibetans, Field Crop, 1-7.

Linder H.P., 1987, The evolutionary history of the poales/restionales: a hypothesis. Kew Bulletin, 42(2): 297-318.

https://doi.org/10.2307/4109686

Liu J., 2014, The phylogenetic relationships among genera and evolution analysis of the Triticeae based on DNA data, Thesis for M.S., Sichuan Agricultural University, Supervisor: Yang R.W., pp. 25-32.

Liu Q., Ge S., Tang H., Zhang X., Zhu G., and Lu B., 2006, Phylogenetic relationships in Elymus (Poaceae: Triticeae) based on the nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences, New Phytol., 170 (2): 411-420.

https://doi.org/10.1111/j.1469-8137.2006.01665.x

Lutz J., Hsam S.L.K., Limpert E., and Zeller F.J., 1995, Chromosomal location of powdery mildew resistance genes in Triticum aestivum L.(common wheat). 2. Genes Pm2 and Pm19 from Aegilops squarrosa L., Heredity, 74(2): 152-156.

https://doi.org/10.1038/hdy.1995.22

Mamone G., Ferranti P., Rossi M., Roepstorff P., Fierro O., Malorni A., and Addeo F., 2007, Identification of a peptide from α-gliadin resistant to digestive enzymes: Implications for celiac disease, Journal of Chromatography B., 855(2): 236-241.

https://doi.org/10.1016/j.jchromb.2007.05.009

Mason-Gamer R., 2004, Reticulate evolution, introgression, and intertribal gene capture in an allohexaploid grass, Syst Biol., 53 (1): 25-37.

https://doi.org/10.1080/10635150490424402

Mason-Gamer R., Orme N., and Anderson C., 2002, Phylogenetic analysis of North American Elymus and the monogenomic Triticeae (Poaceae) using three chloroplast DNA data sets, Genome, 45(6): 991-1002.

https://doi.org/10.1139/g02-065

Piperno D., Weiss E., Holst I., and Nadel D., 2004, Processing of wild cereal grains in the Upper Palaeolithic revealed by starch grain analysis, Nature, 430 (7000): 670-673.

https://doi.org/10.1038/nature02734

Prasad V., Strömberg C.A., Alimohammadian H., and Sahni A., 2005, Dinosaur coprolites and the early evolution of grasses and grazers, Science, 310(5751): 1177-1180.

https://doi.org/10.1126/science.1118806

Pratap A., Sethi G.S., and Chaudhary H.K., 2005, Relative efficiency of different Gramineae genera for haploid induction in triticale and triticale x wheat hybrids through the chromosome elimination technique, Plant Breeding, 124(2): 147-153.

https://doi.org/10.1111/j.1439-0523.2004.01059.x

Rutschmann F., 2006, Molecular dating of phylogenetic trees: a brief review of current methods that estimate divergence times, Diversity and Distributions, 12(1): 35-48.

https://doi.org/10.1111/j.1366-9516.2006.00210.x

Sanderson M.J., 1997, A nonparametric approach to estimating divergence times in the absence of rate constancy, Molecular Biology and Evolution, 14(12): 1218-1231.

https://doi.org/10.1093/oxfordjournals.molbev.a025731

Sanderson M.J., and Doyle J.A., 2001, Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. American Journal of Botany, 88(8): 1499-1516.

https://doi.org/10.2307/3558458

Shan L., Qiao S.W., Arentz-Hansen H., Molberg Ø., Gray G.M., Sollid L.M., and Khosla C., 2005, Identification and analysis of multivalent proteolytically resistant peptides from gluten: implications for celiac sprue, Journal of Proteome Research, 4(5): 1732-1741.

https://doi.org/10.1021/pr050173t

Sharma H.C., and Gill B.S., 1983, Current status of wide hybridization in wheat, Euphytica, 32(1): 17-31.

https://doi.org/10.1007/BF00036860

Silano M., Dessì M., De Vincenzi M., and Cornell H., 2007, In vitro tests indicate that certain varieties of oats may be harmful to patients with coeliac disease, J. Gastroenterol. Hepatol., 22(4): 528-531.

https://doi.org/10.1111/j.1440-1746.2006.04512.x

Thomasson J.R., 1988, Fossil grasses: 1820-1986 and beyond, In International Symposium on Grass Systematics and Evolution, Washington, DC (USA), 27-31 Jul 1986, Smithsonian Institution Press

Weiss E., Kislev M.E., and Hartmann A., 2006, (Perspectives-Anthropology:) Autonomous Cultivation Before Domestication, Science, 312(5780): 1608-1610.

https://doi.org/10.1126/science.1127235

Weiss E., Wetterstrom W., Nadel D., and Bar-Yosef O., 2004, The broad spectrum revisited: Evidence from plant remains, Proc Natl Acad Sci USA., 101(26): 9551-9555.

https://doi.org/10.1073/pnas.0402362101

Zubillaga P., Vidales M.C., Zubillaga I., Ormaechea V., García-Urkía N., and Vitoria J.C., 2002, HLA-DQA1 and HLA-DQB1 genetic markers and clinical presentation in celiac disease, J. Pediatr. Gastroenterol. Nutr., 34(5): 548-554.

https://doi.org/10.1097/00005176-200205000-00014

Zuckerkandl E., and Pauling L., 1965, Molecules as documents of evolutionary history, Journal of theoretical biology, 8(2): 357-366

https://doi.org/10.1016/0022-5193(65)90083-4