A Review of C4 Plants in Southwest Asia: An Ecological, Geographical and Taxonomical Analysis of a Region With High Diversity of C4 Eudicots

Southwest Asia is climatically and topographically a highly diverse region in the xeric belt of the Old World. Its diversity of arid habitats and climatic conditions acted as an important area for the evolution and diversification of up to 20 (of 38 known) independent Eudicot C4 origins. Some of these lineages present unique evolutionary strategies like single-cell functioning C4 and C3–C4 switching mechanisms. The high diversity of C4 taxa in Southwest (SW) Asia is also related to the presence of seven phytogeographic zones including the Irano-Turanian region as a center of diversification of many Caryophyllales lineages and the Somali-Masai region (Southern Oman and Yemen) as a center of diversification for C4 Monocots. Nevertheless, the C4 flora of SW Asia has not received detailed attention. This paper presents a comprehensive review of all known C4 species in the area based on a literature survey, own floristic observations, as well as taxonomic, phylogenetic and herbarium data, and δ13C-isotope ratio analysis. The resulting checklist includes a total number of 923 (861 native, of which 141 endemic, and 62 introduced) C4 species, composed of 350 Eudicots and 509 Monocots, most of which are therophytic and hemicryptophytic xerophytes with pluriregional and Irano-Turanian distribution. Two hundred thirty-nine new δ13C-isotope ratios of C4 and C3 plants, as well as some taxonomic changes are presented. An analysis of the distribution of the three main C4 plant families (Chenopodiaceae, Poaceae, and Cyperaceae) in the region in relation to climatic variables indicates that the increase of C4 species follows more or less a latitudinal gradient similar to global patterns, while separate taxonomic groups seem to depend on specific factors as continentality (Chenopodiaceae), average annual temperature (Cyperaceae), and the presence of summer precipitation (Poaceae). An increase of C4 Eudicots in W-E direction even in similar longitudinal belts is explained by a combination of edaphic and climatic conditions. The provided data should encourage a deeper interest in the evolution of C4 lineages in SW Asia and their adaptation to ecological and climatical conditions and awaken interest in the importance of local C4 crops, the conservation of threatened C4 taxa, and awareness of human impacts on the rapid environmental changes in the region.

Southwest Asia is climatically and topographically a highly diverse region in the xeric belt of the Old World. Its diversity of arid habitats and climatic conditions acted as an important area for the evolution and diversification of up to 20 (of 38 known) independent Eudicot C 4 origins. Some of these lineages present unique evolutionary strategies like single-cell functioning C 4 and C 3 -C 4 switching mechanisms. The high diversity of C 4 taxa in Southwest (SW) Asia is also related to the presence of seven phytogeographic zones including the Irano-Turanian region as a center of diversification of many Caryophyllales lineages and the Somali-Masai region (Southern Oman and Yemen) as a center of diversification for C 4 Monocots. Nevertheless, the C 4 flora of SW Asia has not received detailed attention. This paper presents a comprehensive review of all known C 4 species in the area based on a literature survey, own floristic observations, as well as taxonomic, phylogenetic and herbarium data, and d 13 C-isotope ratio analysis. The resulting checklist includes a total number of 923 (861 native, of which 141 endemic, and 62 introduced) C 4 species, composed of 350 Eudicots and 509 Monocots, most of which are therophytic and hemicryptophytic xerophytes with pluriregional and Irano-Turanian distribution. Two hundred thirty-nine new d 13 C-isotope ratios of C 4 and C 3 plants, as well as some taxonomic changes are presented. An analysis of the distribution of the three main C 4 plant families (Chenopodiaceae, Poaceae, and Cyperaceae) in the region in relation to climatic variables indicates that the increase of C 4 species follows more or less a latitudinal gradient similar to global patterns, while separate taxonomic groups seem to depend on specific factors as continentality (Chenopodiaceae), average annual temperature (Cyperaceae), and the presence of summer precipitation (Poaceae). An increase of C 4 Eudicots in W-E direction even in similar longitudinal belts is explained by a combination of edaphic and climatic conditions. The provided data should encourage a deeper interest in the evolution of C 4 lineages in SW Asia and their adaptation to ecological and climatical

INTRODUCTION
Since its discovery, during the seventh decade of the twentieth century, the C 4 photosynthetic pathway has received attention of extensive studies (Hatch, 1999). In contrast to C 3 photosynthesis, which evolved under high atmospheric CO 2 levels and mesic conditions, C 4 photosynthesis developed under low CO 2 levels and arid conditions. The climatic changes during the Oligocene (30-25 M.y.a.) and the following Miocene, marked by dropping CO 2 levels and increasing seasonality with hot and dry periods and the resulting expansion of arid habitats, favored the convergent evolution and diversification of various C 4 lineages (Sage, 2001;Osborne and Beerling, 2006;Christin et al., 2008;Sage, 2016). C 4 photosynthesis involves a CO 2 concentrating mechanism in hot and arid conditions through the activity of the phosphoenolpyruvate carboxylase (PEPC), an enzyme with a high affinity for HCO − 3 . The mechanism avoids photorespiration by concentrating CO 2 levels around Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) using a special dual compartmentation named Kranz-anatomy (Sage et al., 2012;Bräutigam and Gowik, 2016). This structure allows fixation of CO 2 by PEPC in the mesophyll and its decarboxylation and concentration around Rubisco in the bundle sheath cells. Subsequently, it has been shown, however, that Kranz-anatomy is not always required for C 4 photosynthesis in terrestrial plants (Voznesenskaya et al., 2001).
For the classification as a C 4 plant, the d 13 C ratio is a decisive indicator in all known fully functional C 4 plants. It is related to differences in the fractionation of stable carbon isotopes 12 C and 13 C between C 3 and C 4 plants (O'Leary, 1988;Von Caemmerer et al., 2014). Based on the type of decarboxylating enzymes, C 4 plants have been distinguished according to their metabolic type in NADdependent malic enzyme (NAD-ME)-type, NADP-dependent malic enzyme (NADP-ME)-type, and phosphoenolpyruvate carboxykinase (PEP-CK)-type (Pyankov et al., 2010). Recent studies, however, question this classification, indicating that C 4 plants can be classified in relation to the malate-decarboxylating enzymes as NAD-ME or NADP-ME, while PEP-CK may be considered as an additional decarboxylating pathway Wang et al., 2014;Rao and Dixon, 2016).
C 4 photosynthesis has been a metabolic revolution within the plant kingdom and a highly favorable metabolic pathway in plants growing under hot and arid conditions. In fact, while C 4 plants comprise only 3% of vascular plants, they account for 25% of terrestrial photosynthesis (Sage, 2004;Osborne, 2010). Furthermore, this photosynthetic pathway evolved at least 64 times convergently in different plant families (Sage, 2016). Three most numerous C 4 taxonomic groups can be distinguished: C 4 Poaceae (with around 19 independent C 4 clades including ca. 321 genera and over 5,000 species), C 4 Cyperaceae (including 6 independent C 4 clades in around 7 genera and over 1,300 species) and C 4 Caryophyllales [including 24 independent C 4 clades within 8 families (namely Amaranthaceae s. str., Aizoaceae, Caryophyllaceae, Chenopodiaceae, Gisekiaceae, Molluginaceae, Polygonaceae, and Portulacaceae] ca. 50 genera and over 1000 species) (Sage, 2016). The most interesting case in Caryophyllales is the particular diversity of independent C 4 clades within the Chenopodiaceae family, that may include up to 13 independent C 4 clades and 15 different C 4 leaf anatomical types (Pyankov et al., 2001;Kadereit et al., 2003;Kadereit et al., 2012;Sage, 2016). [Following Hernandez-Ledesma et al., 2015;Walker et al., 2018, Chenopodiaceae is treated in this article as a separate family and not as a part of Amaranthaceae, although APG III and IV suggest it to be included in Amaranthaceae (APG III (The Angiosperm Phylogeny Group), 2009; APG IV (The Angiosperm Phylogeny Group), 2016)].
Previous studies have shown that different taxonomic groups of C 4 plants [e.g., Monocots (Poaceae, Cyperaceae) and Eudicots (Chenopodiaceae)] follow different distributions in relation to climatic variables (Stowe and Teeri, 1978;Pyankov et al., 2010). In the case of the European continent, the distribution of C 4 Monocots seems to be related to high temperatures, while the distribution of C 4 Chenopodiaceae and several other C 4 Eudicot lineages shows a relation to aridity (Pyankov et al., 2010). Similar tendencies can be observed also in other regions. E.g., the adaptation to aridity extends the dominion of C 4 Chenopods to the highly continental Gobi desert and over 4,000 m altitude of the Pamir (Pyankov et al., 2000a). In tropical and subtropical Asia, Africa, Australia, and South America the majority of C 4 Poaceae confirm the trend observed in Europe, being mainly distributed in hot climates with the obligatory presence of summer rainfall (Hattersley, 1983;Cabido et al., 2008;Ehleringer et al., 1987;Schulze et al., 1996;Wooler et al., 2001). C 4 Cyperceae, finally, have been reported to be abundant in warm tropical temporary wetlands (Stock et al., 2004). The biodiversity of C 4 plants has been so far reported for Europe (Pyankov et al., 2010) and China (Wang and Ma, 2016), while further studies on the distribution of C 4 plants in relation to climatic and ecological parameters are available for various C 4 lineages or specific geographical areas of the Old and New World (Raghavendra and Das, 1976;Teeri and Stowe, 1976;Tieszen et al., 1979;Waller and Lewis, 1979;Winter, 1981;Hattersley, 1983;Ehleringer et al., 1987;Batanouny et al., 1988;Medina et al., 1989;Schulze et al., 1996;Akhani et al., 1997;Rundel et al., 1999;Pyankov et al., 2000a;Wooler et al., 2001;Stock et al., 2004;Cabido et al., 2008;Mantlana et al., 2008).
The C 4 flora of Southwest Asia is of great interest because of the remarkable diversity of C 4 Eudicots and discovery of singlecell functioning C 4 (Rechinger, 1963(Rechinger, -2015Nikitin and Geldikhanov, 1988;Akhani et al., 1997;Edwards et al., 2004;Akhani and Ghasemkhani, 2007). Southwest (SW) Asia in an extended sense including the Middle East, European parts of Turkey, Transcaucasia, Turkmenistan, Afghanistan, and Pakistan presents a topographically very diverse region.
Southwest and Central Asia have been proposed to be the origin of at least 20 of the 38 accepted C 4 Eudicot lineages (Sage, 2011;Kadereit and Freitag, 2011;Sage, 2016). In fact, both regions can be considered an exceptional areas for the evolution and diversity of C 4 Eudicots in a predominantly Monocot dominated "C 4 world." This and the high diversity of ecological and morphological features and adaptations of SW Asian C 4 plants, as well as the quick degradation of the arid regions in the Middle East by improper agriculture, overgrazing, water mismanagement, desertification, and climate change (Motagh et al., 2008;Akhani, 2015b) and finally the need of detailed information on the C 4 taxa of this region, inspired compilation of this work.
The aims of this work are: 1) to present an "as complete as possible" checklist of C 4 species of SW Asia, with information on their respective ecological, floristic, and anatomical characteristics, where available; 2) to publish new d 13 C stable isotope ratios for taxa with previously unpublished isotope data; 3) to analyze the distribution of C 4 plants in SW Asia in relation to climatic variables and to evaluate different adaptations of the three main taxonomic groups of C 4 plants (Chenopodiaceae, Cyperaceae, Poaceae) in relation to climate; 4) to discuss shortly the economical and ecological importance of major regionally cultivated or wild growing C 4 crops in a region highly affected by climate change and desertification.
The biodiversity of C 4 plants of Southwest Asia is of particular interest to comprehend the evolutionary history of C 4 plants and the interaction of habitats, biogeographic regions, climate and soil in relation to C 3 _ C 4 domination. This allows to understand and predict future scenarios of the arid belts of the world, affected by global warming.

Data Collection and Nomenclature
In this article, we treated SW Asia in an extended way ( Figure 1). The geographical area considered in this article (extended Southwest Asia) includes the territories of the following countries and geographic areas: Afghanistan, Armenia, Azerbaijan, Bahrain, Iran, Iraq, Israel/Palestine, Jordan, Kuwait, Lebanon, Oman, Pakistan, Qatar, Saudi Arabia, Sinai Peninsula, Syria, Turkey, Turkmenistan, United Arab Emirates, and Yemen ( Figure 1). The C 4 species distribution data, habitat, and altitude preferences used for compilation of the checklist of C 4 plants of SW Asia were obtained from standard floras, regional contributions, revisions, monographs, reports, and data bases and electronics sources (Supplementary Appendix Table 1). Data from Herbarium collections were obtained from the Herbarium of H. Akhani (Halophytes and C 4 Plants Research Laboratory, School of Biology, University of Tehran), the Royal Botanic Garden Edinburgh Herbarium (E), and the Herbarium of Russian Academy of Sciences-V. L. Komarov Botanical Institute (LE). Finally, we received some unpublished data such as Cyperaceae of the Arabian Peninsula, kindly provided by Dr. David A. Simpson through personal communications (Royal Botanical Gardens Kew).
The published literature has been screened for all C 4 species in the area, their respective habitat, distribution, life form, choro-, morpho-, and ecotypes. Taxonomic treatment and nomenclature of the C 4 species were mainly based on global databases such as IPNI (2019) and POWO (2019). The naming of families followed the Angiosperm Phylogeny Group classification (APG IV, 2016) with the exception of the family Chenopodiaceae, which is treated as a separate family and not as a part of Amaranthaceae following Hernandez-Ledesma et al. (2015). The polymorphic genus Calligonum was treated taxonomically in accordance with the taxonomic simplifications proposed by Soskov (2011) and the genus Tribulus according to the simplifications proposed by Thomas and colleagues (Al-Hemaid and Thomas, 1996;Varghese et al., 2006) (see Discussion for further notes). Plants were classified as C 4 species based on stable carbon isotope ratios (d 13 C-values) as far as previous or own data support, leaf anatomy (presence of Kranz-anatomy), and biochemical subtypes (Supplementary Appendix Table 1). Species with no specific data available, but taxonomically belonging to pure C 4 clades, were as well included in the list but marked with AR (analysis required). The C 4 biochemical subtypes are based on published literature (Supplementary  Appendix Table 1). In many cases we have extrapolated the "deduced" subtypes based on respective lineage unless there are evidences of multiple subtypes. Furthermore, species with lacking data, belonging to genera with both C 4 and C 3 clades and unknown attribution were preliminarily excluded from the list and listed separately (Supplementary Table 2). Life form, eco-and morphotype categorization for each species were based on the above-mentioned sources and/or own observations. The consideration of a species as native or introduced was based on distribution data and indications from the standard sources. Chorotypes were proposed based on a species distribution data in relation to the boundaries of the phytochoria. We used the phytogeographical system suggested for SW Asia and Africa by White and Leónard (1991) and considered other references such as Zohary (1973); Takhtajian (1992); Miller and Cope (1996); Djamali et al. (2012); Welk (2015) (Figure 1).

d 13 C Analysis
A total of 234 plant samples (Supplementary Appendix Table 1) with unpublished d 13 C-values ( 13 C/ 12 C ratios) have been sampled from herbarium samples. The d 13 C were analyzed according to the standard procedure relative to PDB (Pee Dee Belemnite) limestone as the carbon isotope standard and calculated according to this formula: d = 1,000 x (R sample / R standard − 1) (Osmond et al., 1975;Akhani et al., 2009). The samples have been fine ground using a Retsch ball grinder and transferred in microtubes for isotopic measurement. Each sample was weighted to a mass between 1.50 to 1.90 mg at the SSMIM Mass Spec Lab of the National Museum of Natural History of Paris and burnt in an automated combustion system (EA Flash 2000 Thermo device), interfaced with a DeltaV Advantage Thermo isotope ratio mass spectrometer (continuous flow). The analytical uncertainty within each run estimated from repeated analyses of our laboratory standard (alanine, normalized to IAEA caffeine-600) was lower than 0.08‰ (k = 1) for d 13 C values.

Climate Data and Statistical Analysis
For the correlation of C 4 taxonomic group distributions within the study area and climatic variables, bioclimatic data were extracted from the Worldwide Bioclimatic Classification System (Rivas-Martinez and Rivas-Saenz, 1996Djamali et al., 2011). For a few stations we obtained climatic data of the Iranian Meteorological Organization (IRIMO) and Scholte and De Geest (2010) and Raza et al. (2015) (Supplementary Figure  1). Variables, representative for the SW Asia, have been extracted and/or calculated: a. Mean annual daily temperature (T) b. Mean annual precipitation (P) c. Continentality index [I c =T max (mean temperature of warmest month) − T min (mean temperature of coldest month)] d. De Martonne Annual Aridity Index [P/(T+10)] e. Duration of dry season (number of months with P<2T) f. Mean summer precipitation (P s -mean precipitation of warmest 3 months) FIGURE 1 | The study area includes Southwest (SW) Asia in an extended sense ( Figure 1). Phytogeographic boundaries after White and Leónard (1991). We considered 29 weather stations for the evaluation of distribution of main C 4 taxonomic groups in relation to climate. The two extreme climatic conditions showing winter rainfall regime (Tehran) and summer rainfall regime (Lahore) are shown. All other climatic diagrams are depicted in Supplementary Figure 1. g. Ombrothermic index of summer (Ios 3 =P p3 /T p3 *10), where P p3 is the precipitation of the whole summer and T p3 the sum of the mean temperatures for each month of the summer).
The distribution and diversity of C 4 plants in relation to climatic variables (annual mean daily temperature, annual mean precipitation, De Martonne aridity index, continentality index, mean summer precipitation, duration of dry season, and ombrothermic index of summer) has been calculated by linear correlation analysis. The correlation is considering the number of total C 4 plant species, as well as the numerically and ecologically most important taxonomic groups of C 4 plants, e.g., number of C 4 Poaceae, C 4 Cyperaceae and C 4 Chenopodiaceae, and the C 4 Monocot/Eudicot ratio. The data have been imported into "OriginPro," which has been used to calculate the linear correlation and Pearson correlation coefficient and for graphical design (Origin Pro, 2017).

RESULTS
A complete list of all SW Asian C 4 species with life form, chorotype, ecotypes, d 13 C-values, metabolic and Kranz anatomical subtypes is presented in Supplementary Appendix Table 1.

General Statistics
A total number of 923 (861 native and 62 introduced) C 4 species belonging to 166 genera, 48 independent C 4 lineages, 19 families, and 9 orders have been known from extended SW Asia (Supplementary Appendix Table 1, Figure 1). For the taxonomic diversity of SW Asian C 4 plants view Figure 2.
In the case of Polycarpaea (a polyphyletic genus with both C 3 and C 4 species), we have only included one species in our list, considering the fact that we could not verify the photosynthetic pathway of seven additional species, reported from the area (mostly from Socotra). A list of these species is given in the Supplementary Table 2.

Distribution of C 4 Species by Country
The number of native and introduced C 4 species in individual SW Asian countries/regions and respective Monocot/Eudicot proportions are shown in Figures 3 and 4 respectively. The highest diversity of C 4 plants has been documented for Pakistan (account for 43% of all known native SW Asian species), Yemen (38%), Iran (36%), Saudi Arabia (36%), Afghanistan (30%), and Oman (28%), respectively. The differences in the proportion of C 4 Monocot/Eudicots allowed us to categorize countries into three groups: 1) countries with remarkably high percentage of C 4 Eudicots, such as Turkmenistan and Iran; 2) countries with more or less equal proportion of Monocot/Eudicots such as Armenia, Azerbaijan, Afghanistan, Turkey, Syria, Iraq, and Sinai Peninsula; 3) counties with higher percentage of C 4 Monocots, that is all other countries located in southern parts of the region.
The countries with the highest number of introduced C 4 plants are Israel and Palestine with 50 introduced species, Jordan with 39 introduced species, and Pakistan with 30 introduced species respectively. The percentage of C 4 plants in relation to total number of recorded plant species per country is highest in Kuwait (23%), Bahrain (22.5%), Qatar (22%), and Oman (20%), respectively ( Figure 5).

C 4 Endemics of Southwest Asia
One hundred forty-one C 4 species (36 Monocots and 105 Eudicots, 93 of which are Chenopodiaceae) are endemics of SW Asia; 74 of those (22 Monocots and 52 Eudicots) are strict "country endemics." The highest number of "country endemics" are documented in Iran (27 species), Yemen (14 species, 9 of which are endemic to the island of Socotra), Afghanistan (8 species), and Oman (7 species), respectively. The highest number of endemism occurs in Chenopodiaceae (93 species) and Poaceae (31 species). The three endemic richest genera (with 10 or more endemic species) are Halothamnus (12 endemic sp. in SW Asia), Halimocnemis, and Climacoptera (respectively 10 endemic sp. in SW Asia).
The only generic C 4 endemic of the area is the monotypic genus Halarchon (Halarchon vesiculosum) restricted to Afghanistan. Except a few old records outside of SW Asia, the range of three known species of Bienertia is limited to this area.

Climate Correlation
The species-richness of C 4 Chenopodiaceae increases with increasing continentality and decreases with increasing mean summer precipitation ( Figures 6A, E). The C 4 richness of Cyperaceae increases with increasing mean annual temperature and is negatively affected by increasing continentality ( Figures  6B, G). The number of C 4 Poaceae increases with increasing mean annual daily temperature ( Figure 6H). Totally, the diversity and abundance of C 4 plants increases with increasing annual daily temperature and duration of the dry season and decreases with increasing continentality ( Figures 6C, F, I).
Finally, the prevalence of Monocots over Eudicots is related to increasing average summer precipitation ( Figure 6D).

Life Forms and Ecotypes
Life forms and ecotypes of the C4 plants are shown in Figures  7A, B.

Phytogeographic Distribution of C 4 Species of Southwest Asia
The phytogeographic distribution of C 4 species of SW Asia are shown in Figure 7C.

Southwest Asia Center of Origin of Major C 4 Flora
The checklist appended in this paper has been compiled with great caution to include as much data as available, thanks to intensive Flora compilation in SW Asian countries published during more than half a century (Rechinger, 1963(Rechinger, -2015Davis, 1966Davis, -2001Guest andGhazanfar, 1966-2013;Nasir andAli, 1970-2003;Nikitin and Geldikhanov, 1988;Miller and Cope, 1996) and intensive botanical explorations in the region. However, as a first contribution, it requires more data to fill some gaps on local flora of the Levant (Syria, Jordan and Lebanon) and the absence of up-to-date information on specific groups such as Cyperaceae in the Arabian Peninsula.
In spite of our efforts to check photosynthetic types of all putative C 4 groups, we could not get enough samples for a few Polycarpaea species. The preliminary phylogenetic studies show that Polycarpaea is polyphyletic including both C 3 and C 4 species. It has been suggested to segregate C 4 species in a separate genus Polia (Kool, 2012). Within our area, however, only Polycarpaea corymbosa (L.) Lam. is a reliable C 4 species. Some other SW Asian species such as P. repens (Forsskal) Aschers. and Schweinf., P. spicata Wight ex Arn., P. hassalensis Chamberlain, and P. haufensis A.G. Miller) have been reported to be C 3 according to Kool (2012) and a few ones (Supplementary Table 3) require further investigation.
So far 174 species of Calligonum have been described worldwide (Soskov, 2011), however phylogenetic studies and attempts to barcode these species revealed little information to support this diversity (Tavakkoli et al., 2010;Li et al., 2014;Doostmohammadi et al., 2020). We followed the recent monography of the genus which accepts a wide species concept including only 28 species and 8 interspecific hybrids (Soskov, 2011) and recent minor changes by Shi et al. (2016). The polymorphic, mainly Saharo-Sindian genus Tribulus, has been partly reviewed for India and Saudi Arabia by synonymizing many species (Al-Hemaid and Thomas, 1996;Varghese et al., 2006). A systematic review of the genus in our area is highly welcome.
Despite recent progress in the taxonomy and phylogeny of Chenopodiaceae (Kadereit et al., 2003;, still there are ambiguities in monophyly of some genera such as Hammada. The phylogenetic tree based on combined nuclear and chloroplast markers showed polyphyly of three species Hammada articulata, H. salicornica, and H. griffithii Schüssler et al., 2017). In a long debate on the nomenclatural status of the Kali-clade within Salsoleae which has been separated from Salsola s.l. based on strong molecular and morphological data, recent unexpected decision on replacing the type of the genus Salsola by Salsola kali L. instead of S. soda by International Code of Nomenclature (Akhani et al., 2014;Mosyakin et al., 2017;Turland et al., 2018) resulted in instability and chaos of all names used since 2007. Therefore, in order to keep phylogenetic classification of Salsoloideae we are pushed to change the name of many species traditionally classified in Salsola into Soda (see Nomenclatural Appendix). Furthermore, we provide new combinations for some species which have been overlooked in the phylogenetically based system of Salsoleae by .
Based on our data (Table 1), the C 4 flora of SW Asia includes 923 (ca. 11% of world known C 4 species) and represent 48 of 65 known C 4 lineages of the world (Sage, 2016;Kadereit and Freitag, 2011). The area, as one of the major center of diversity of C 4 Eudicots, harbors the origin of ca. 19 C 4 Eudicot lineages and has representatives of all families known to have C 4 species either as native or introduced (Sage, 2016) ( Table 1, Supplementary Appendix Table 1).
SW and Central Asia which represent largely the Irano-Turanian flora are the center of origin of at least 12 C 4 Chenopodiaceae lineages Sage, 2011;Sage, 2016). We consider Salsoleae s. str. as one C 4 origin with understanding that present topologies suggest two additional origins that are not well resolved Kadereit and Freitag, 2011).

C 4 Eudicots Are Related to Dominance of Continentality Index
Our findings show different tendencies of C 4 Monocot and C 4 Eudicot distributions in the study area. The usual pattern of increase of C 4 species along a latitudinal gradient is more or less similar to global patterns (Pyankov et al., 2010, Figure 6) with deviations mostly due to its complex topography, edaphic factors, and the resulting presence of specific microclimates. The C 4 grasses increase along the southern and eastern edges of the region (Yemen, Oman, Pakistan) with higher summer precipitation due to monsoon and tropical climates (Ghazanfar and Fisher, 1998), Figure 6D. In fact, C 4 -grasslands are known to depend on a dry and rain seasonality, where bushfires during dry seasons on one hand prevent forest growth while high temperatures on the other hand favor C 4 grasses (Skinner et al., 2002;Bond et al., 2005;Keeley and Rundel, 2005;Hoetzel et al., 2013). The savanna-like C 4 grasslands at the south-eastern corner of the Caspian forests are supported by a small peak of summer precipitation, while the spring flora is dominated by C 3 grasses and forbs (Akhani and Ziegler, 2002). The C 4 poor but rainfall rich Euro-Siberian portions of SW Asia also favor C 4 Monocots over C 4 Eudicots. For example, in the north-western edges of the study area the percentage of Monocot species in the local C 4 flora may reach 84% (Zaqatala, Republic of Azerbaijan) ('GBC').
The high proportion of C 4 Eudicots in Iran and Turkmenistan may be explained by large saline and sandy deserts and high continentality, which favor halophytic Chenopodiaceae species and psammophytic Calligonum spp. The increase of C 4 Eudicots in W-E direction even in similar longitudinal belts may be explained by a combination of edaphic and climatic conditions (compare the opposite tendency in China, Wang and Ma, 2016). Indeed, the continentality index clearly increases along a W-E direction over the SW Asia to Central Asia (Djamali et al., 2011;Djamali et al., 2012). The harsh summer times with scarcity of fresh water resources in deserts of Iran and Turkmenistan reduce the competitive advantages of C 3 species (Pyankov et al., 2010;Sage and Sultmanis, 2016). Additionally, absence of summer rainfall supresses C 4 grassland formation. Although higher continentality adversely affects general C 4 domination ( Figure  6C), this is not the case for C 4 Chenopodiaceae, which are adapted to temperate deserts with continental climate ( Figure  6A). This is explained by the phenology of chenopods with an estival active growing season (Toderich et al., 2007). Many chenopods and species of Calligonum are highly specialized by their morpho-anatomical and physiological traits to live under harsh conditions (e.g., their long root systems have access to the underground and subsurface water-table) (Gintzburger et al., 2003;Soskov, 2011). The negative correlation of C 4 Cyperaceae with continentality ( Figure 6B) and positive correlation with average annual temperature relate to their sensitivity to low winter temperatures (Wang and Ma, 2016). C 4 Cyperaceae however do not seem to be unaffected by precipitation. The later may be explained by a high variety of ecotypes within C 4 Cyperus (the main bulk of C 4 Cyperaceae), ranging from psammophytic xerophytes to hygrophytes limited to permanent wetlands and the consequent species shift in relation to various ecological conditions. Finally, it is interesting to note, that while different metabolic subtypes often indicate the adaptation of C 4 Monocots to specific ecological conditions, e.g., NADP-ME Monocots are more likely distributed in areas with high rainfall, while NAD-ME Monocots grow in conditions with lower rainfall (Schulze et al., 1996), this feature doesn't seem indicative in C 4 Eudicots E.g., xerophytic C 4 chenopods show both NAD-ME or NADP-ME metabolisms (see Supplementary Appendix Table 1).
Southwest Asia-Center of Biodiversity of Single-Cell C 4 and C 3 -C 4 Switching Plants One of the fascinating aspects of C 4 photosynthesis is the discovery of Single-Cell functioning C 4 photosynthesis in two C 4 lineages of the Chenopodiaceae (Voznesenskaya et al., 2001;Edwards et al., 2004;Akhani et al., 2005). This photosynthetic type was described for the first time in Suaeda aralocaspica (Bunge) Freitag and Schütze (= Borszczowia aralocaspica Bunge), a hygrohalophyte from the saline depressions of Central Asian semideserts (Freitag and Stichler, 2000;Voznesenskaya et al., 2001). Bienertia as a monophyletic lineage in which all species perform single-cell functioning C 4 was discovered shortly after S. aralocaspica with some new species (Voznesenskaya et al., 2002;Akhani et al., 2003;Akhani et al., 2005;Kapralov et al., 2006;. The genus Bienertia is diversified mostly in Iran and some surrounding areas often on moist and highly saline soils in association with several annual C 4 chenopods belonging to Caroxylo-Climacopteretea class in the interior Iran or on open habitats of saline shrublands on the lowlands around the Persian Gulf between Tamarix species or on tidal shores (Akhani et al., 2003;Akhani et al., 2009).
Instead of a conventional system of C 4 terrestrial species, having a dual-cell compartment consisting of mesophyll and bundle sheath cells, in both single-cell C 4 lineages, this achieved by localizing photosynthetic machinery in a single-cell type. In Suaeda aralocapica dimorphic chloroplasts are polarized in a single layer mesophyll cell, in which the proximal chloroplasts fix CO 2 using PEPC into a C 4 acid which moves to distal chloroplasts via a cytoskeleton network (Edwards et al., 2004;Chuong et al., 2006). Similarly, the Bienertia species single-cell system has a unique form in which lateral chloroplasts function as mesophyll cells and a bubble-like central chloroplast compartment (CCC) acts as Kranz-cells in usual C 4 species. This discovery stimulated scientists to deeply investigate the biology and genomics of this simplified system, which might have advantages for those looking for genetic engineering of C 4 photosynthesis in C 3 crop plants (Schuler et al., 2016).
Another peculiarity within the C 4 plants of SW and Central Asia, is the presence of two types of photosynthesis within the life cycles of particular lineages and species of Chenopodiaceae. In these species C 3 cotyledon leaves are replaced by C 4 shoots. This characteristic is widespread in the subfamily Salsoloideae and rarely in Suadedoideae (Pyankov et al., 1999;Pyankov et al., 2000b;Pyankov et al., 2001;Akhani and Ghasemkhani, 2007). In both tribes of Salsoleae and Caroxyleae several genera, such as Haloxylon, Halothamnus, Hammada, Girgensohnia, Noaea and Soda inermis (Salsola soda), Climacoptera, Halimocnemis, Petrosimonia, Kaviria, and Halocharis are known to have this switching mechanism. In Suaedoideae, this type was known in Suaeda microphylla evidenced by carbon isotope values (Akhani and Ghasemkhani, 2007) or anatomy (Khoshravesh and Akhani, unpublished data). As this characteristic is of interest for gene engineering, the transcriptomes of Haloxylon ammodendron and Soda inermis (Salsola soda) have been studied (Li et al., 2015;Lauterbach et al., 2017).
Ecologically, the development of a switching mechanism from a C 3 to a C 4 photosynthetic metabolism hasn't however received much attention. Switching chenopods are mainly halophytes and xerohalophytes of continental temperate saline ecosystems (Climacoptera, Petrosimonia, Halimocnemis, Soda inermis), gypsiferous (Halothamnus), and sandy (Haloxylon) habitats of the Irano-Turanian floristic region and are taxonomically among the main and most biodiverse taxa of SW Asian C 4 Eudicots. Switching plants are also among the main biomass producers in the Irano-Turanian deserts, suggesting that the switching mechanism may imply an evolutionary advantage to those species. The continental climates of their habitats may probably favor a switching mechanism and the presence of C 3 cotyledons at early developmental stages, when germination at low temperatures favors the presence of C 3 cotyledons while increasing temperatures during the growth period favor C 4 leaves (Akhani and Ghasemkhani, 2007). Further investigations however are needed to comprehend better the ecological advantages in comparison with tropical deserts.

Palaeoclimatic Implications
The distribution pattern of C 4 plants in SW Asia is at least partly related to the palaeoclimatic conditions which have prevailed in the region during the Neogene. Today, the region is dominated by the summertime subtropical anticyclones (Zarrin et al., 2009) which induce a long summer drought in most parts of SW Asia. The subtropical anticyclonic system is particularly intensified and maintained by the high elevations in SW Asia (Zarrin et al., 2011) which are mostly present since at least 7 million years ago (Djamali et al., 2012). During the late Neogene, a long summer drought has thus dominated over the region impeding the penetration of moisture-bearing westerlies into the Irano-Anatolian inlands and Central Asia. The continental inlands of SW Asia, although close to the Indian Ocean, receive no monsoon precipitation during the summertime because of the complex monsoon-desert mechanism described by Rodwell and Hoskins (1996). The palaeoclimatic archives suggest that excepting the Arabian Peninsula, most of the continental interior of SW Asia has not received summer monsoon rainfall during the intensification phase of the latter at the beginning of the Holocene (Djamali et al., 2010). Only SE Iran might have received some direct summer precipitation from the summer monsoons some 11,400 to 6,500 years ago (Vaezi et al., 2019). Some of the C 4 plant communities found in currently dry areas of S Iran and Arabian Peninsula (see above) may be the relicts of formerly widespread C 4 communities when the area received more summer rainfall. Relatively higher values of d 13 C of organic matter in the Jazmurian playa sediments during the early Holocene ( Figure 8A in Vaezi et al., 2019) may indeed reflect the important contribution of more abundant C 4 grasses during the Indian Monsoon intensification phase in SE Iran. With the exception of increasing summer rains in SE Iran and Arabia, it seems thus that most of SW Asia has always been subjected to long summer droughts and high continentality since several million years (Djamali et al., 2012). Such long-lasting geoclimatic conditions are characterized by strong continentality, long summer droughts and presence of intracontinental endorheic basins which support the formation of a broad range of saline environments suitable for the diversification and specialization of C 4 Eudicots in particular the halophytic chenopods.

Human Utilization of C 4 Plants in Southwest Asia
SW Asia including the Fertile Crescent had a long history of plant domestication and land use (Zohary and Hopf, 2000). Deserts and steppe populations utilize many C 4 species in a variety of ways, as source for food, fire wood, for grazing, construction, greening of their surroundings, medicine, and in recent times for desert reclamation programs and afforestation. They have additional potentials such as usage as biofuel, genetic engineering practices and even invention of new crops. C 4 crops exploited in SW Asia either natively originated or widely distributed or imported from other parts of the world together with their main applications are listed in the Supplementary  Table 4. It has to be noted, that although the wild forms of many C 4 crops, like Eragrostis tef, Echinochloa frumentacea, Panicum miliaceum, Eleusine coracana, Setaria italica, Soda inermis, etc. are distributed throughout SW Asia, they are mostly cultivated outside of this region.
The most important and most species rich group of C 4 crops are millets and millet-like cereals cultivated traditionally for their grain in arid areas of S Asia and Africa. Among them several major millet crops like sorghum (Sorghum bicolor) (Sanjana Reddy, 2017a), proso millet (Panicum miliaceum) (Gomashe, 2017), foxtail millet (Setaria italica) (Hariprasanna, 2017), and pearl millet (Cenchrus americanus) (Sanjana Reddy, 2017b) made it to fame out of their region of domestication and have been introduced not only to SW Asia but are extensively cultivated worldwide for their grains. Sweet sorghum (Sorghum bicolor) is also an alternative source of syrup and sugar (Sanjana Reddy, 2017a), although the main pantropical sugar crop remains the extensively cultivated sugarcane (Saccharum officinarum) (James, 2014). Although the wild forms of small millets, are distributed in SW Asia, they are mainly cultivated as traditional cereals of cultural significance outside of this area (Seetharam and Riley, 1986). In fact, they form important grain crops in the traditional communities of S Asia and Subsaharan Africa. An interesting example is cultivation of teff (Eragrostis tef) concentrated in Ethiopia and Eritrea, where it is of the most important crop plants and is used mainly for the production of traditional Injera flat bread (Seetharam and Riley, 1986). Teff recently however is wining fame as a healthy alternative cereal outside of E Africa. Molecular studies have shown that this allotetraploid is closely related to Eragrostis pilosa, growing in SW Asia (Ingram and Doyle, 2003;Assefa et al., 2017).
Millets cultivated on smaller scales in SW Asia include finger millet (Eleusine coracana), Indian barnyard millet (Echinochloa frumentacea), Japanese millet (E. esculenta), and adlay millet (Coix lacryma-jobi). Their cultivation in SW Asia is mainly limited to regions where they bear cultural significance, such as the plains and hills of Afghanistan and Pakistan (Breckle and Rafiqpoor, 2010;Breckle et al., 2013). Corn (Zea mays) is the world's most important C 4 grain crop and SW Asia is not an exception, where it is extensively cultivated (Staller, 2010).
Many wild SW Asian C 4 grasses are important fodder and pasture crops, for biomass production or used for landscape greening on large and small scales in arid areas of N America, Australia, S Europe, Central Asia, India, and Subsaharan Africa, namely Bouteloua curtipendula, Cenchrus spp., Chloris gayana, Cynodon dactylon, Diplachne fusca, Lasiurus scindicus, Panicum antidotale, Setaria viridis, Sorghum halepense and Sporobolus spp. They may present a source for further millet and forage grass breeding and cultivation for forage and erosion control in disturbed and desertifying areas of SW Asia.
The C 4 Monocots are of high importance for summer grazing of wildlife such as Persian Ibex or livestock on steep rocky outcrops and disturbed or degraded South Caspian forests (Akhani and Ziegler, 2002). Grazing on salt marsh grasslands dominated by Aeluropus is common in most parts of the region (Whigham et al., 1993).
Haloxylon persicum, H. ammodendron, Xylosalosla richteri, and Calligonum spp. may yield up to 1.2 t, 3.0 t, 1.3, and 1.2 t green biomass per hectare respectively, depending on habitat type and population density. Haloxylon ammodendron is definitely the largest species by biomass and can reach a height of up to 9 m and an age of up to 100 years (Fet and Atamuradov, 1994;Gintzburger et al., 2003) ( Figure 8K).
Additionally, psammophytic Xylosalsola sp. in Turkmenistan and Central Asia and Soda stocksii (Salsola stocksii) and Hammada salicornica in Pakistan and India are grown for the same purpose. Haloxylon ammodendron is mainly cultivated in Central Asia, SE Europe, NW China, and Iran for as erosion control and forage on salt and clay deserts, saline flats, and saline sands. From the Mediterranean toward Iran Atriplex spp. like A. halimus and A. canescens are cultivated for the same purpose on saline clayey soils (Hanelt, 2001;Danin, 2007;Walker et al., 2014). Bassia prostrata has been cultivated in Turkmenistan, Central Asia, Europe, and the USA as forage and erosion control on clayey, slightly saline, sandy, and rocky soils (Dzyubenko and Soskov, 2014).
With climate change, overpopulation and resource mismanagement, SW Asia is highly in need of alternative, drought, and salt resistant crops to make agriculture more sustainable. A series of C 4 crops, in addition to those already introduced and cultivated in SW Asia, are highly interesting for further introduction into cultivation, since their wild forms are already distributed and adapted to SW Asian climate conditions.

Conservation
Being mainly part of the so-called MENA Region (Middle East and North Africa), SW Asia with its xeric climates is highly susceptible to climate change (Pal and Eltahir, 2016). Although future scenarios vary, concerning the degree of climatic changes, a general consensus on the increase of mean temperatures and heat extremes exist (Evans, 2009;Waha et al., 2017). The same is regarding the decrease of precipitation and increase of drought and aridity, with the exceptions of the southern shores of SW Asia, where the increase of monsoon precipitation due to a shift of the inter-tropical convergence zone is expected to occur according to some predictions (Waha et al., 2017;Byrne et al., 2018). The effects of climate change are enhanced by growing population and an aggressive mismanagement of water and land resources. For example, in Iran an ineffective irrigation agriculture, extensive dam construction and groundwater overuse has led to a significant decrease of groundwater levels and the drying and destruction of the main lake, river, and wetland ecosystems (Motagh et al., 2008;Madani, 2014;Akhani, 2015b;Motagh et al., 2017). On the other hand, the SW Asian C 4 flora, although highly specialized, is very susceptible to minor changes in many extreme habitats (groundwater levels, period, and amount of precipitation, etc.).
Of the 923 C 4 species of SW Asia, 141 (105 Eudicot and 36 Monocots-15.3%) are endemic to SW Asia, while 70 species (50 Eudicots and 20 Monocots-7.6%) are strict country endemics with very limited habitats. However, even some species distributed beyond SW Asia (e.g., several Cyperus species described from limited areas of the Somali-Masai floristic region) show very restricted distributions. The strict country endemics can be grouped mainly in two subgroups: a) C 4 Eudicots (mainly chenopods) mainly endemic to habitats of the Irano-Turanian floristic region; b) C 4 Monocots (mainly Poaceae) endemic to the Somali-Masai floristic region (of those the half of the species are endemic to the island of Socotra). Under high climatic and anthropogenic pressure on the narrow habitats of SW Asian C 4 endemics, many such species are critically endangered.
As an example, the recently discovered Bienertia kavirense Akhani ( Figure 10J), restricted to a narrow region within Iran's central saline desert, has been declared critically endangered from its discovery . According to our own documentation in a saline flat located 60 km W of Tehran near Rude Shur (saline river), a very dense subpopulation of Bienertia cycloptera in 2003 completely disappeared in 2009 (Akhani et al., 2003;Akhani, 2016;Akhani and Rudov, 2018) apparently due to dropping of underground water levels. This tragic situation is observed in many similar habitats, where dropping of underground and subsurface water levels affects soil moisture and is consequently a threat for existence of many C 4 annuals.
Recent field trips of the authors discovered, that the narrow habitats of Halimocnemis alaeflava and Halimocnemis azerbaijanensis have been fragmented and partly destroyed by factory construction, complete removal of upper soil layers, as well as road and dam construction. In fact, if further localities of H. alaeflava are not discovered in future, there is a probability of its complete extinction as its type habitat is on the way toward complete destruction. Another critical example is a subpopulation of the local endemic Caroxylon abarghuense ( Figure 10K) in Touran Biosphere Reserve, located in Central East of Iran. In a small valley dominated by Tamarix shrubs, only 16 living individuals of C. abarghuense have been found. Their seeds do not seem germinable probably because allee effect resulted from small size population. A subpopulation of Piptoptera turkestana, discovered in 1989 on sandy dunes of central Iran, ca. 30 km ESE of Kashan, could not be recollected in the same place after extensive searches and apparently disappeared from the locality probably due to habitat disturbance and oil mulching ( Figure 11A). Several taxa (e.g., Climacoptera zenobiae) lack proper assessment and are known from very limited collection samples. Species like Climacoptera czelekenica Pratov, being island endemics, depend on the changing water level of the Caspian Sea. On the island of Socotra, the high number of endemic plants is threatened by both climate change and overgrazing (Attorre et al., 2007;Rejzek et al., 2016). This directly affects also the C 4 endemics of Socotra, being all C 4 grasses. Conservation of endangered C 4 endemics is further complicated by the lack of proper population assessment in many regions of SW Asia because of lacks of interest and founding and specially because of inaccessibility due to long lasting military conflicts. The two of the four most endemic rich countries (Afghanistan and Yemen) are both long time battle grounds.
Additional threats to the local C 4 flora are introduced and invasive C 4 plants. The introduced C 4 flora of SW Asia (68 species) is mainly composed of Poaceae (34 species), Amaranthaceae sensu stricto (20 species), and Euphorbiaceae (7 species) (Pahlevani et al., 2020). Several C 4 lineages not typical for the region have been introduced to SW Asia (C 4 Flaveria clade A, C 4 Alternanthera, and Gomphrena). The genus Amaranthus, although a neophytic genus in most areas of SW Asia, includes not only recently introduced species but also apparently old neophytes (e.g., A. blitum) and local species (e.g., A. graecizans, A. tenuifolius, A. sparganicephalus). Of the 67 introduced C 4 species at least 48 have been reported to be invasive in various regions of the world ("CABI-Invasive Species Compendium. Wallingford, UK: CAB International"; Elmore and Paul, 1983). These species may form a major threat to local floras and economic burdens for agriculture and livestock. An important aspect of invasiveness in the area is introducing C 3 invasive species into C 4 habitats. This happened in S Iran and Pakistan where introduction of Prosopis juliflora occupied many of the habitats of drought resident species including native C 4 species.
The saline areas, sandy dunes, and marl or gypsum habitats, where the majority of C 4 Eudicots grow, have no protection priority in most of the countries of SW Asia. Mostly, these habitats are considered as badlands with poor biodiversity. Grazing and shortage of water are big problems affecting the vegetation in such habitats. Therefore, most of these lands with poor vegetation cover are converted into dust emission centers with a huge environmental concern (Akhani, 2015b). An example of mismanagement of such habitats we refer to intensive oil mulching in many sand dunes in Iran with dense C 4 plant vegetation. Such activities which aim to control dune movement result in destroying natural flora with many C 4 annuals and shrubs ( Figure 11A). Sadly, improper managements threatened many gypsophytic, halogypsophytic, and xerophytic hill habitats, which are the main habitats of endemic C 4 chenopods (Akhani, 2006;Ghorbanalizadeh et al., 2020) (Figure 11B). We strongly recommend re-evaluation of protection policies to restore and protect C 4 -rich habitats that are of high advantage in desert areas because of their low water requirements and vegetation cover provision during harsh seasons.

CONCLUSIONS
SW Asia is not only an area of origin and diversification of most interesting and highly adapted C 4 Eudicot lineages, but also provide diverse and vast habitats for growing C 4 Monocots. The evolution of various eco-morphological traits among C 4 Eudicots lineages (notably single-cell functioning C 4 plants and switching C 3 -C 4 species) and the presence of many endemic species are indicative of long-lasting ecological pressure that supports speciation and specialization among different families in particular Chenopodiaceae and Calligonum (Polygonaceae).
The C 4 Eudicots are known to dominate vast Irano-Turanian deserts. Our data suggest, that this is mainly related to the adaptation of C 4 Eudicots to the continental climatic conditions of the Irano-Turanian deserts in contrast with the C 4 Poaceae, that dominate areas with the presence of summer rainfall in the southern and southeastern parts of the area influenced by monsoon summer rains.
Unfortunately, the SW Asian C 4 plant diversity is threatened by the impact of intensive land use synergized by global warming and rapid desertification. In spite of our knowledge on the taxonomy and phylogeny of many C 4 lineages, many questions regarding SW Asian C 4 plants are however still unresolved. For example, the taxonomy of the genera Calligonum, Climacoptera, Hammada, Kaviria, Caroxylon, and Tribulus needs still to be clarified. More studies are necessary to understand the phylogenetic relationships of C 3 and C 4 species of the genera Fimbristylis, Polycarpaea and clarify ambiguities in presence of some C 3 and C 3 -C 4 intermediate lineages within prevalently C 4 Salsoloideae (Chenopodiaceae). The study of the vegetation of some neglected areas and the description of some specific C 4 plant dominated communities as well as the compilation of some country floras in the region (e.g., Syria, Jordan) would be highly informative.
Due to political instability and low interest in the conservation of desert areas with lower biodiversity, several rare C 4 endemics are under the threat of extinction. Being part of the ecologically and climatically vulnerable MENA region, SW Asia is also in need of a sustainable management of water resources and agriculture. The C 4 dominated habitats requires protection priority and monitoring of highly adapted plants to harsh environments. We re-emphasize the importance of regional C 4 crops and the selection of new C 4 crop candidates with lesser ecological impact than genetic engineering as a much more sustainable approach to guarantee the food security facing the future global change.

DATA AVAILABILITY STATEMENT
The original contributions presented in the study are included in the article/supplementary material; further inquiries can be directed to the corresponding author.

AUTHOR CONTRIBUTIONS
AR provided the data, wrote the first draft, prepared all figures and tables. HA planned and supervised the research, contributed to the preparation of the data and text, provided all photos, edited the text and jointly worked together in writing of first draft. MM analyzed all the carbon isotopes in the paper, read, and edited the manuscript. MD contributed to the writing of the palaeoecology part of the paper.

FUNDING
This research was funded by postdoctoral support for the first author by the International Office of the University of Tehran and the Erasmus Mundus Marhaba Program. personal communication on the Cyperaceae of the Arabian Peninsula and Socotra, Targol Chatrenoor for her advices on the list of Climacoptera species and Roxana Khoshravesh for her critical suggestion to improve this paper.

SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2020. 546518/full#supplementary-material SUPPLEMENTARY APPENDIX TABLE 1 | Complete List of C4 plants in Southwest Asia showing their C 4 lineage, life form, chorotype, endemism, ecotype, d 13 C and C 4 subtype and respective leaf or shoot anatomical type.
SUPPLEMENTARY FIGURE 1 | Climatic diagrams of selected 29 stations in different parts of SW Asian countries obtained from of the Iranian Meterorological Organization (IRIMO), Scholte and De Geest (2010) and Raza et al. (2015).