Shattercane ( Sorghum bicolor (L.) Moench Subsp. Drummondii ) and Weedy Sunﬂower ( Helianthus annuus L.)—Crop Wild Relatives (CWRs) as Weeds in Agriculture

: Shattercane ( Sorghum bicolor (L.) Moench subsp. drummondii ) and weedy sunﬂower ( Helianthus annuus L.) are two examples of crop wild relatives (CWRs) that have become troublesome weeds in agriculture. Shattercane is a race belonging to a different subspecies than domesticated sorghum ( Sorghum bicolor (L.) Moench subsp. bicolor ). Weedy sunﬂower populations are natural hybrids between wild and domesticated sunﬂower ( Helianthus annuus L.). Both species have key weedy characteristics, such as early seed shattering and seed dormancy, which play an important role in their success as agricultural weeds. They are widely reported as important agricultural weeds in the United States and have invaded various agricultural areas in Europe. Shattercane is very competitive to sorghum, maize ( Zea mays L.), and soybean ( Glycine max (L.) Merr.). Weedy sunﬂower causes severe yield losses in sunﬂower, maize, soybean, pulse crops, and industrial crops. Herbicide resistance was conﬁrmed in populations of both species. The simultaneous presence of crops and their wild relatives in the ﬁeld leads to crop–wild gene ﬂow. Hybrids are fertile and competitive. Hybridization between herbicide-tolerant crops and wild populations creates herbicide-resistant hybrid populations. Crop rotation, false seedbed, cover crops, and competitive crop genotypes can suppress shattercane and weedy sunﬂower. Preventative measures are essential to avoid their spread on new agricultural lands. The development of effective weed management strategies is also essential to prevent hybridization between sorghum, sunﬂower, and their wild relatives and to mitigate its consequences.


Introduction
Crop wild relatives (CWRs) are wild plant species closely related to domesticated crops. According to Maxted et al. [1], the genetic relationships between crops and CWRs are described by the following taxa groups: TG1a-crop taxon; TG1b-the same species of crop; TG2-the same series or section of crop; TG3-the same subgenus of crop; TG4-the same genus of crop; and TG5-the same tribe, but different genus of crop. The species in taxa groups TG1a, TG1b, TG2, and TG3 are of unique interest from both plant breeding and weed science perspectives because they belong in the primary gene pool of a genus (GP-1) and can successfully interbreed [2][3][4][5].
These wild taxa are valuable genetic resources that should be explored for use in plant breeding programs. They can increase genetic diversity in cultivated species through stigma (in the flowers of the crop's wild relatives). The male gametophytes (e.g., pollen grains) rapidly rehydrate and begin to germinate [40]. Subsequently, a pollen tube grows through the pistil tissues of the stigma and style, across the surface of the placenta, and then through the micropyle of the ovule to reach the female gametophyte in the embryo sac [40,41]. The growth of the pollen tube stops, and two gametes are released [40]. It should be noted that pollen tube growth is both polar and directional. Cytosolic Ca 2+ ions are thought to play an important role in pollen tube formation, growth, and polarity as secondary messengers [40,42,43]. In any case, the physical distance between crop plants and their wild relatives and the synchrony of their flowering times are crucial factors affecting hybridization rates [18,37].
The current study summarizes information on weedy relatives of crops that are problematic weeds in agriculture because they compete with a wide range of crops, have high invasive potential, and can also successfully interbreed with their closely related domesticated crops and generate complex weed problems [32]. Regarding species selection, it should be noted that shattercane and weedy sunflower are problematic species in a wider range of crops compared to weedy rice. Moreover, the interactions between weedy rice and rice and the appropriate strategies to control weedy rice in direct-seeded rice fields were recently studied [15,19]. Therefore, the present study focused on the weedy relatives of sorghum and sunflower, i.e., shattercane and weedy sunflower, respectively. Although the selected species are known to be important weeds mainly in the United States, there is much evidence that they have also invaded various agricultural areas in Europe [44,45].
First, we present information on the origin of these species and also on their important morphological and ecological traits. Then, we summarize information on their competitive ability against their closely related domesticated species and also against other important summer field crops. In addition, we include information about their occurrence in Europe where they have the potential to become serious invaders in the future. Cases are presented where herbicide resistance was confirmed. Evidence of successful hybridization between crops and their wild relatives is included along with information on the fitness of the hybrids produced; we also include cases where crop-wild gene flow led to the development of herbicide-resistant hybrids. Weed management strategies that can be effective in controlling these species are discussed. Emphasis is also placed on the role of weed management in preventing gene flow from crops to their wild relatives.
As for the other species of the Eu-sorghum subgenera, S. propinquum is a diploid (2n = 20), rhizomatous, biennial to perennial, wild species [52]. S. halepense is another rhizomatous perennial wild species, which is tetraploid (2n = 40), also known as john-songrass [52]. This species is thought to have arisen either by natural hybridization between S. bicolor × S. propinquum or by chromosome duplication in S. propinquum [14,53]. Regarding S. almum, it is a tetraploid (2n = 40), rhizomatous, perennial species and is a natural hybrid between S. bicolor × S. halepense [54]. Of the perennial species presented, S. propinquum and S. almum are not reported as troublesome weeds [16]. In contrast, johnsongrass is one of the most common and noxious weeds in agriculture, which can also reduce biodiversity due to its high invasive potential [55].
This article could focus on both shattercane and johnsongrass, as both species are troublesome weeds that can hybridize with the crop [2,3]. However, the present study focuses on species that belong to the primary gene pool (GP-1) of a genus and have very strong genetic links to the crop. Species in this primary gene pool readily interbreed and produce fertile hybrids [16]. In contrast, species belonging to the secondary gene pool (GP-2) of a genus can also interbreed with the crop, but successful gene transfer between these two gene pools can be difficult in some situations. Since shattercane belongs to the primary gene pool (GP-1) of sorghum while johnsongrass belongs to the secondary gene pool (GP-2) of the genus [2], further information is provided only on shattercane. In addition, the main aspects of johnsongrass biology and ecology, as well as its negative impacts on agriculture and biodiversity, were already summarized in a previous study [5].

Morphological and Ecological Traits
Shattercane is a warm-season annual grass that originated in Africa [46]. The plants have erect, unbranched stems and can grow 1-4 m tall. This weedy race has some key characteristics that explain its evolution into a troublesome weed. First of all, plant height cannot be regulated in shattercane because it lacks a dwarfing trait that is controlled in cultivated sorghum by four recessive dwarfing genes [56]. Therefore, the increased canopy height results in lower harvest index values and makes mechanical harvesting an impossible task [21]. It should also be noted that the great height of shattercane improves its ability to compete with tall cereals such as maize (Zea mays L.) and increases its ability to disperse seeds over long distances [57].
As for seed dispersal, it is an ecological trait playing a central role in the success of this species as an agricultural weed. Seed dispersal is rapid, and the explanation lies in the abscission layer that forms at the base of the spikelet at the stage of physiological seed maturity. This abscission layer allows the seed to detach from the panicle and immediately fall to the soil surface. It is worth mentioning that only a light breeze (e.g., a wind moving at a very low speed of 7-12 km h −1 ) is adequate to cause seed shattering before the cultivated crop can be harvested [14]. In addition, the shattered seeds can stay dormant for a long time in the soil and remain viable. Burnside et al. [58] reported a seed survival period of up to 13 years in the United States while Fellows and Roeth [59] found that the dormancy period can be further extended if the seeds are tightly enclosed in the glumes. As for the reproductive ability of shattercane, plants typically produce 1-6 panicles with each panicle producing 500-1500 seeds [57]. An interesting fact is that shattercane has an extended emergence window since the seeds can germinate late in the growing season. These later-emerging weeds may exhibit aggressive growth rates, reach maturity, and produce seeds that enrich the species' seedbank dynamics in the soil [14].

Competitive Ability and Distribution
Shattercane populations can establish on agricultural land, field margins, and marginal areas in various regions across the world. Its presence as a weed was reported in North America, in Africa where it is believed to have originated, in Asia, and also in Europe [16,27,44,46,49,60]. Shattercane infestations result in significant yield loss in important summer field crops including grain sorghum, maize, and soybean. All reports of yield loss due to shattercane competition are from field trials conducted in the United States, with the exception of the case study by Raey et al. [27], which was conducted in Iran, Asia (Table 1). Especially in the United States, shattercane is one of the most common and problematic weeds in grain sorghum [50]. There are also case studies from this continent showing the competitive ability of shattercane against domesticated sorghum and other important summer field crops. In sorghum, early studies revealed that 5.6 shattercane plants m −2 , spaced 45 cm apart, caused a 73-82% yield loss in grain sorghum [61]. The competitive advantage of shattercane compared to grain sorghum growth was also recently highlighted in greenhouse studies [21,31,36,64,65]. In most of the case studies mentioned, shattercane exhibited a more aggressive growth compared to grain sorghum and the weeds were significantly taller than the domesticated plants. Shattercane is also reported as a strong competitor to maize and soybean. In particular, Beckett and Stoller [49] found that 13 to 20 shattercane plants m −1 of row resulted in a 22% grain yield loss in maize. Seasonlong shattercane interference (from 20 plants m −2 ) reduced grain yield by 43-85% in the study by Hans and Johnson [51]. The same authors also observed significant yield reductions when shattercane was left uncontrolled until it was 31 cm tall. At a density of 6.6 plants m −2 , Deines et al. [26] predicted a grain yield loss of 19%. King and Hagood [64] found that shattercane competition (at a density of 40 plants m −2 ) resulted in up to 34% grain yield loss. In soybean (Glycine max (L.) Merr.), seed yield decreased by more than 60% due to full-season competition by 3.3 shattercane plants m −1 of the row [65]. There is also evidence from Asia showing that 50 soybean plants m −2 were outcompeted by 12 shattercane plants m −2 and suffered a 57% loss in seed yield [27].
There are not many official reports on the presence of shattercane in Europe. However, it should be noted that in the context of climate change, the resilient and versatile sorghum has gained importance as a multipurpose crop in Europe [66]. Sorghum acreage has increased in all European sorghum producing countries, namely France, Italy, Hungary, Romania, Bulgaria, Austria and Greece [67]. Defelice [14] pointed out that shattercane can spread anywhere in the world where domesticated sorghum is grown. Therefore, it is possible that populations of shattercane have developed in the European countries mentioned above, although this is not officially reported. The U.S. Department of Agriculture (USDA) has conducted a weed risk assessment for this weed species and concluded that the presence of shattercane in sorghum producing countries is underreported because it is difficult to distinguish shattercane from sorghum [68]. Berenji and Dahlberg [44], Dahlberg et al. [69] and Schwartz-Lazaro and Gage [70] mention that there are at least two distinct areas where shattercane populations were reported, namely southeastern Hungary and northeastern Serbia. Dahlberg et al. [69] also included a photograph of a shattercane population growing in a broom corn field in their study. Broomcorn is a cultivated race of sorghum whose panicles are used as raw material for making natural corn brooms [71]. The morphology of shattercane is very similar to broom corn. Since Europe, especially Hungary, Romania and Serbia, are the main producers of broom and broom corn in the world [44], it is logical to assume that populations of broom corn may have developed in these areas but are not yet reported due to the morphological similarities between broom corn and shattercane. In view of this situation, a research goal of weed scientists in Europe should be to carefully survey sorghum fields to detect populations of shattercane and take action to control this weed before it becomes established in Europe.

Herbicide Resistance
Research has shown that consecutive applications of ALS (acetolactate synthase)inhibiting herbicides in a particular field inevitably result in the selection of ALS-resistant shattercane populations (Table 2). Anderson et al. [72] reported shattercane resistance to primisulfuron-methyl in a biotype collected from a maize field treated with primisulfuron-methyl and nicosulfuron for three consecutive growing seasons. In the study by Lee et al. [73], shattercane populations from 12 fields were resistant to primisulfuron-methyl and nicosulfuron. In the same study, another population was susceptible to primisulfuron-methyl and nicosulfuron but resistant to imazethapyr. The presence of a biotype with noticeable levels of resistance to primisulfuron and cross-resistance to nicosulfuron and imazethapyr was also confirmed [74]. Resistance evolved after 10 years of use of ALS-inhibiting herbicides in a field where maize was rotated with soybean. Zelaya and Owen [75] observed that one population was 29 times more resistant to imazethapyr compared to a sensitive population. These authors noted that resistance occurred in an environment where the use of ALS-inhibiting herbicides was an important component of the selection pressure. In another study, the continuous use of nicosulfuron for weed control in silage maize resulted in the selection of a shattercane population that was resistant to nicosulfuron and exhibited cross-resistance to imazethapyr and imazapyr [64]. Werle et al. [76] screened 190 shattercane populations and observed five and four populations that were resistant to imazethapyr and nicosulfuron, respectively, and two populations that were cross-resistant to nicosulfuron and imazethapyr. All of these cases of herbicide resistance in shattercane were reported in the United States. However, if shattercane becomes a serious invader in European fields, crop rotation and herbicide rotation practices should be used to prevent the development of herbicide-resistant populations.

Hybridization with Domesticated Sorghum
Both shattercane and sorghum belong to the primary gene pool of the genus, they are sexually compatible, and can be wind pollinated. Therefore, these sympatric species can successfully outcross under favorable field conditions and produce fertile hybrids [21,36,60]. Schmidt et al. [37] highlighted flowering duration of sorghum and flowering overlap between the two species as important factors determining hybridization rates in the field. The same authors also emphasized the crucial role of wind speed and direction in the outcome of the hybridization process [37]. Moreover, hybridization rates tend to increase when the distance between interacting populations becomes smaller [3,37]. Another noteworthy point is that gene transfer from the crop to its wild relatives is more frequent than gene transfer in the opposite direction [77]. One possible explanation is that populations of domesticated plants in agricultural fields are usually much larger, and the domesticated plants, therefore, produce larger amounts of pollen compared to their wild relatives [77].
In any case, hybrids between sorghum and shattercane can be competitive, as shown by case studies where successful hybridization was reported. Sahoo et al. [36] found that grain sorghum × shattercane hybrids produced 31% more biomass and were 56-61% taller compared to grain sorghum. They also found that the hybrids produced 40-63% and 42-61% more spikelets per panicle and seeds per plant, respectively, compared to their domesticated parents. In this study, hybrid relative fitness was similar to shattercane as also observed in the study by Schmidt et al. [37]. In the study by Magomere et al. [78], F 1 hybrids produced 1509 more seeds than their parent plants, while the mean seed weight of the hybrids was 41% higher than that of grain sorghum. Similar observations were made for aboveground biomass production and tillering capacity, indicating a competitive advantage of the F 1 hybrids over their domesticated parents [78]. Schmidt et al. [21] revealed also that F 2 hybrids are characterized by lower vegetative growth and fecundity than shattercane but their relative fitness can be comparable to that of grain sorghum. In particular, these authors reported no significant differences between grain sorghum and grain sorghum × shattercane F 2 hybrids in the number of panicles per plant, aboveground biomass production, and seed production [21]. In the pot experiments by Werle et al. [31], F 1 hybrids outcompeted an ALS-resistant grain sorghum inbred line and caused a biomass yield loss of 75-95%. Aside from their competitive ability, seed dormancy is another characteristic of these hybrids that might enable them to be highly persistent on agricultural lands. Indeed, there is evidence that seed dormancy is similar to shattercane and seeds can survive in the soil for many years [3,21,36].
Another consequence of hybridization between domesticated sorghum and its wild relative, shattercane, is the emergence of herbicide-resistant hybrids under certain circumstances. First, it should be noted that in the past, germplasm from shattercane populations with resistance to ALS-inhibiting herbicides was used to develop the 'Inzen' technology, i.e., to develop ALS-tolerant grain sorghum populations [79]. Werle et al. [63] revealed that most of herbicide-resistant shattercane populations have evolved independently and resistance is not the result of pollen-mediated gene flow between ALS-tolerant grain sorghum and shattercane. However, there is evidence that possible outcrossing between the crop and its wild relative may indeed result in the creation of ALS-resistant grain sorghum × shattercane hybrids. For instance, Werle et al. [23] found that shattercane × ALS-tolerant grain sorghum hybrids were tolerant to ALS-inhibiting herbicides and herbicide application did not reduce hybrid growth. Adugna and Bekele [60] also reported that such hybrids can be tolerant to herbicides and at the same time competitive against grain sorghum and exhibit similar fitness to shattercane. In another study conducted under greenhouse and real field conditions, the creation of ALS-tolerant hybrids was confirmed as the hybrids were not affected by the application of a nicosulfuron plus rimsulfuron mixture and maintained their competitive advantage over their ALS-tolerant grain sorghum parents [31].

Origin
The genus Helianthus is native to the temperate zones of North America and includes 52 species and 19 subspecies with 14 annuals and 39 perennials. The basal chromosome number is n = 17. All 14 of the annual species are diploid (2n = 34), while in the group of perennial species there are 26 diploid, 3 tetraploid (2n = 68), 7 hexaploid (2n = 102) and 3 mixaploid species [80,81]. Taxonomically, there are four distinct sections in the genus, namely the annual polyphyletic section Helianthus, the annual monophyletic section Agrestis, the perennial polyphyletic section Ciliares with two races, and the perennial polyphyletic section Divaricati with four races [82]. The species Helianthus annuus L. of the section Helianthus includes the domesticated sunflower (Helianthus annuus L. var. macrocarpus) cultivated for its oil seeds and also its weedy or wild forms [83].
In an early study by Heiser [84], it was suggested that there are three subspecies of H. annuus, namely H. annuus subsp. lenticularis, H. annuus subsp. texanus, and H. annuus subsp. annuus, the last subspecies being emphasized as the weedy sunflower. However, there are still no official names for the subspecies. In another study, Heiser [83] emphasized that H. annuus exhibits high morphological variability, so that its wild and weedy relatives cannot be adequately classified into separate subspecies. This is in contrast to the genus S. bicolor, where shattercane is a race belonging to a different subspecies than the domesticated sorghum. Indeed, there is strong evidence that the weedy forms of H. annuus are not represented by a specific subspecies but are the natural result of hybridization with domesticated sunflower. There is evidence of crop introgression in weedy sunflowers since they combine wild and domesticated traits in proportions that vary between wild and domesticated plants [4,[85][86][87][88]. In some recent studies, the various forms of H. annuus are divided into the domesticated sunflower, the weedy sunflowers, which include the "agrestal" biotypes, and the wild sunflowers, which include the "ruderal" biotypes. The term "agrestal" is used to describe plants evolved under selection pressure on agricultural land while the term "ruderal" refers to plants inhabiting naturally disturbed sites [89].
For the species H. annuus, the weedy "agrestal" biotypes are considered natural cropwild hybrids [4,13,20,22]. The initial invasions of such biotypes on agricultural land might be attributed to importations of contaminated sunflower seed lots. The importations of contaminated seed from the United States were the dominant hypothesis for the spread of weedy sunflowers in European fields [38,86,87]. As for the wild "ruderal" biotypes, their spread into non-crop areas such as roadsides, water channels, firebreaks, etc., is thought to be promoted by anthropogenic activities [39,85,90,91]. The ruderal biotypes can hybridize recurrently with the domesticated plants leading to the spread of highly competitive hybrids in the field [4,39,92]. Although seed transport by humans is considered to explain the invasion of weedy sunflowers in South America, the role of ruderal biotypes in the spread of weedy forms in these regions and also in North America is highlighted [88,[92][93][94]. For instance, Kane and Rieseberg [94] attributed the development of multiple weedy sunflower populations in the United States to the presence of ruderal populations near cultivated sunflower fields. Several factors favor the hybridization process including the overlapping flowering periods of domesticated and wild sunflower, the self-incompatibility trait of wild sunflower, and the presence of shared pollinators under real field conditions [34]. In addition, pollen transfer from the crop to wild plants can occur even from 1 km away [18].

Morphological and Ecological Traits
Various forms of H. annuus occur as domesticated sunflowers, as weeds in agriculture and as wild plants on naturally disturbed, uncultivated sites. Domesticated sunflowers have unbranched stems of 1.2-2.0 m tall, topped by a single, large-diameter yellow-colored head. In addition, anthocyanins are not present in the plant tissues [83,84]. However, weedy sunflowers have taller stems characterized by apical or full branching. Unlike domesticated plants, weedy sunflowers form several heads per plant, usually between 17 and 34. Head diameter, seeds per head, 1000 seed weight, and seed oil content are significantly lower compared to cultivated sunflowers. Head color can be red or yellow. Anthocyanins are found in the stem, petioles, and stigma. Research has shown that the morphology of weedy sunflowers is intermediate between wild biotypes and domesticated sunflowers [4,13,39,86,88]. The wild trait of self-incompatibility and the domesticated trait of male-sterility can be also observed [34,86].
Seed dormancy is an important ecological trait of weedy sunflowers that enables seed bank formation on agricultural lands. In greenhouse tests conducted by Presotto et al. [17] with five weedy sunflower populations, seed dormancy reached 77% when no stratification treatments were applied. In another recent study, weedy sunflower seeds remained viable and dormant in the soil for 42 months, suggesting that such biotypes form persistent seedbanks and even establish on agricultural lands outside their native range [20]. Seed dormancy and seedbank formation are traits that originated in wild populations and were transferred to weedy sunflowers through crop-wild hybridization [17,20,86,95,96]. On top of seed dormancy, the seed shattering ability of weedy sunflowers contributes to their success as agricultural weeds. The seeds are easily detached from the heads due to the anatomy of the disks, which are characterized by a lower depth-width ratio compared to domesticated sunflowers, replenishing the seed bank of weedy sunflower in the field [4,92]. As for seed production, it can range between 2200 and 6460 seeds per plant [22,97,98]. Presotto et al. [30] found that the fitness and seed production of weedy sunflowers can be significantly reduced compared to their domesticated and wild parents. However, the same authors found that relative fitness and fertility of plants tended to increase when weedy sunflowers were backcrossed with cultivated or wild sunflower populations.

Competitive Ability and Distribution
Weedy sunflowers were reported as agricultural weeds in their native range, i.e., in North America, South America and particularly Argentina, and also in several countries in Europe [22,25,86,98,99]. Their competitive ability is attributed to their early-season vigor, rooting, and vegetative growth, plant height, and allelopathic potential [13,100,101]. There are several reports highlighting the detrimental effect of weedy sunflower interference on the yield performance of summer field crops (Table 3).
In the three-year field trials conducted by Casquero et al. [13] in Argentina, sunflower seed yield loss surpassed 50% due to weedy sunflower interference at the density of 4 plants m −2 . At higher density, i.e., 10.7 plants m −2 , weedy sunflower reduced sunflower seed numbers per plant, 1000 seed weight and seed yield per plant by 66, 41, and 80%, respectively [22]. As for the presence of weedy sunflowers as agricultural weeds in the United States, Deines et al. [26] found that weedy sunflower was 11 times more competitive than shattercane and predicted a yield loss of 46% for maize due to competition from 4 weedy sunflower plants m −2 . In the study by Falkenberg et al. [99], competition 20-25 plants m −2 reduced maize net return by 66-68% compared to the case where weedy sunflower was controlled by herbicide application. In soybean, the presence of 3 plants m −2 reduced seed yield by 47-72% compared to weed-free conditions [24]. Geier et al. [100] noticed that weedy sunflower interference at a density of 4.6 plants m −2 resulted in almost complete seed yield loss. In another study, weedy sunflower caused a 94% reduction in seed yield under real-field conditions and reduced soybean height and biomass under greenhouse conditions [101]. In pulse crops, Mesbah et al. [102] observed that 1.5 weedy sunflower plants per m of row reduced the dry bean (Phaseolus vulgaris L.) seed yield by 27-34% and also that weedy sunflower was far more competitive than green foxtail (Setaria viridis (L.) Beauv.). Moreover, cowpea [Vigna unguiculata (L.) Walp.] biomass was reported to decrease by 77-82% in the presence of 6 weeds m −2 [28]. In cotton (Gossypium hirsutum L.), season-long interference resulted in complete yield loss at densities of 5, 10, 20, and 50 weedy sunflower plants m −2 [25]. As for another industrial crop, competition from 6, 12, 18, and 24 plants per 30 m of row was reported to reduce the root yield of sugar beet (Beta vulgaris L.) by 40, 52, 67, and 73%, respectively [103]. These authors also found that weedy sunflower was more competitive than velvetleaf (Abutilon theophrasti Medic.). In northeastern Mexico, Rosales-Robles et al. [104]   There is also evidence that weedy sunflower has invaded European fields in recent years. Infestations were observed mainly in the Mediterranean and Balkan Peninsula countries. In France, Muller et al. [86] recorded significant losses in seed yield (35-60%) of sunflower when grown in competition with 12-15 weedy sunflower plants m −2 . The same authors found 12 weedy sunflower populations in a total of 300 sunflower fields studied in Andalusia, Spain. In the same prefecture, Poverene and Cantamutto [105] detected weedy sunflower infestations at a density of 5-7 plants per 100 m 2 in a sunflower field and also detected weedy sunflower patches in uncultivated areas near sunflower fields. In Central Italy, weedy sunflower plants were found in sunflower, maize, sugar beet, processing tomato, alfalfa (Medicago sativa L.), and tobacco (Nicotiana tabacum L.) fields. The most severe infestations were observed on the moist margins of arable fields where tillage and herbicide treatments were limited or absent [106]. There are no official reports of weedy sunflower in Greece. However, farmers have recently complained about the presence of weedy sunflower plants in sunflower fields in the sunflower growing area of Domokos in Central Greece. According to these unofficial descriptions, the weedy plants are present at densities of 3-6 plants m −2 and exhibit typical weedy characteristics, such as branching and the formation of multiple heads with smaller diameters compared to cultivated sunflower hybrids (personal communication; unpublished data). Field surveys will be conducted at these sites to further investigate the development of weedy sunflower populations and also to quantify the effects of competition from weedy sunflowers on sunflower productivity under Greek soil and climatic conditions.
Elsewhere in the Balkan Peninsula, Saulic et al. [107] observed three weedy sunflower populations in northern Serbia, and the different populations showed variability in several morphological characteristics. Bozic et al. [108] conducted field experiments at two sites in Central Serbia where weedy sunflower populations occurred. These authors found that crop-to-weed gene flow was possible and depended on flowering time overlap, wind speed and direction, and also on the distance between the domesticated and wild plants. Stojićević et al. [45] demonstrated that weedy sunflower is a highly invasive species in Serbia, occurring at almost 200 sites with sunflower, maize and spring wheat. These authors found heavy infestations at some sites (20-30 plants m −2 ) and reported that weedy sunflower can produce about 50-100 small-sized heads per plant (10,000-20,000 seeds per plant). Vrbnicanin et al. [98] studied three populations collected from Central Serbia and found that two populations were potentially resistant to nicosulfuron. According to Bozic et al. [108] and Vrbnicanin et al. [98], this species is also considered invasive in Croatia, Romania and Hungary. As for its occurrence on Central Europe, this weed was detected in sunflower fields and adjacent uncultivated areas on Czech Republic [109].

Herbicide Resistance
In addition to their competitive ability, weedy sunflower populations have developed resistance to several herbicides (Table 4). Sunflower Imazamox ALS Inhibitor Imidazolinone [30] Sunflower Imazapyr ALS Inhibitor Imidazolinone [115] The herbicide-resistant populations may be naturally selected following consecutive applications of herbicides with the same mode of action in a particular field. Resistance may also occur as a result of gene flow between herbicide-tolerant domesticated sunflower and its wild relatives.

Natural Selection of Herbicide-Resistant Weedy Sunflower Populations
In the USA, resistance to imazethapyr was confirmed in a population found in a soybean field treated with this herbicide for seven consecutive years [110]. Baumgartnen et al. [111] reported that these biotypes exhibited cross-resistance to imazamox, thifensulfuron-methyl, and chlorimuron-ethyl. Allen et al. [112] observed reduced sensitivity to imazethapyr, imazaquin, imazamox, chlorimuron-ethyl, cloransulam-methyl, and flumetsulam. These populations were collected from a soybean field where chlorimuronethyl was consecutively applied to control weedy sunflower in the past. White et al. [113] found a population that was 9 and 39 times more resistant to chlorimuron-ethyl and imazethapyr, respectively, compared to a sensitive population. This population was collected from a field where these herbicides were applied for eight years in rotation for the control of weedy sunflowers in soybean. Zelaya and Owen [75] noticed that a population was 36 and 43 times more resistant to imazethapyr and chlorimuron-ethyl, respectively, compared to a sensitive population. In addition, seven weedy sunflower populations were recently reported to have evolved resistance to glyphosate in fields where glyphosateresistant maize and cotton were planted for several growing seasons [114].
It should be noted that the cases of herbicide resistance mentioned above were reported from the United States. As for Europe, Vrbnicanin et al. [98] collected two sunflower populations in Serbia from fields treated with nicosulfuron in consecutive years. These authors found that the application of nicosulfuron at the recommended field dose had no effect on the relative fitness and fecundity of the two potentially resistant populations. Although this is not an official case where herbicide resistance was confirmed in dose-response experiments, these results suggest that herbicide-resistant weedy sunflower may be evolving in Europe.

Herbicide Resistance as a Gene-Flow Consequence in H. annuus
Following the introduction of "Clearfield" technology, there is increasing consideration of the spread of imidazolinone-resistant weedy sunflowers in the USA and Europe. This technology was developed in 2003 to create sunflower hybrids with resistance to imidazolinone herbicides and to allow farmers to selectively control broadleaf weeds in the crop; imazamox is the only active ingredient registered for this purpose in the USA, while imazamox and imazapyr are approved in Europe [115]. However, there is evidence that these herbicide-resistant sunflower genotypes can successfully interbreed with wild populations that are present near a cultivated field, leading to the creation of imidazolinone-resistant weedy sunflower populations. Resistance to imazamox, for example, was reported by Massinga et al. [116] in the United States, while Presotto et al. [30] confirmed resistance to imazapyr in Argentina. In such populations, seed dormancy is not affected by hybridization. Seed production, although low in some cases, can increase rapidly when weedy sunflowers backcross with domesticated and wild sunflowers [30,98]. Another consequence of backcrossing is the successful transfer of herbicide resistance traits from weedy sunflowers to wild populations. These herbicide-resistant wild populations can encroach on new cultivated sunflower fields, hybridize with the crop, and generate new populations of herbicide-resistant weedy sunflowers [116].

Proactive Strategies
Weed management should initially rely on the introduction of proactive strategies that prevent the spread of weeds to new agricultural lands [117,118]. Although the spread and establishment of these species is primarily facilitated by early seed shattering, lateemerging individuals may reach maturity at crop harvest [4,14]. Given the morphological and phenological overlap between these crops and their weedy relatives, weed seeds may be harvested when crops are harvested, resulting in seed lot contamination. As a result, shattercane and weedy sunflower can enter new sorghum and sunflower fields, respectively, as seed lot contaminants [39,63]. The machines used for seedbed preparation, sowing and harvesting, and threshing of grains and seeds should be carefully cleaned before moving them from one field to another [13,19]. In addition, systematic scouting of sorghum and sunflower fields for early detection of shattercane and weedy sunflower is crucial when weed density is low. When weedy populations are well established, their control is almost impossible [63,86]. Such proactive strategies prevent the spread of both species, their hybridization with domesticated sorghum and sunflower, and mitigate the consequences of gene flow between crops and their weedy relatives [76,119].
Another important measure to prevent gene flow is the management of crop volunteers and feral populations along field margins and in non-crop areas. To define the two terms: volunteers are crop plants derived from the unintentional loss of seeds during harvest [34]. The germination of these seeds creates populations of crop volunteers that can either grow in subsequent crops in the same field or migrate into field margins and adjacent non-crop areas. In the latter case, populations of a domesticated crop that escape from the field, survive, and successfully reproduce in unmanaged ecosystems are referred to as feral populations [33]. Feral sorghum and sunflower populations can successfully interbreed with shattercane and weedy sunflower, respectively, if they are located at the edge of an infested field [3,34]. The gene flow that occurs from feral to weedy individuals can be very problematic. In sorghum and sunflower fields infested with shattercane and weedy sunflower, respectively, gene flow may be reduced or not occur at all if there is no overlap in flowering time between crops and their weedy relatives. In such cases, flowering overlap may occur between feral populations in field margins and weedy populations growing in the agricultural field. Consequently, gene flow continues to occur. In other words, feral populations derived from volunteer crop plants can potentially serve as genetic bridges for gene transfer between crop plants and their weedy relatives [34].
Herbicide application is the most effective practice to control shattercane and weedy sunflower in field margins and non-crop areas. Glyphosate may be the most effective active ingredient enabling broad spectrum weed control in marginal areas [5]. However, overreliance should be avoided to prevent the development of glyphosate resistant weeds as recently observed in weedy sunflower populations [114]. To maintain its efficacy over time, alternative weed control options in non-crop areas should gain interest. For instance, recent research has shown that natural, environmentally friendly, non-selective herbicides can be effective on annual weeds if applied repeatedly in early weed growth stages [120].

Reactive Strategies
Once shattercane and weedy sunflower infestations are observed on agricultural land, reactive strategies for their management include the use of cultural practices, herbicides, and mechanical methods. Effective weed management is essential to avoid yield loss in a variety of summer field crops (including sorghum and sunflower) and also to prevent crop-weed gene flow in sorghum and sunflower fields.

Cultural Practices
Crop rotation is a cultural practice that increases crop diversity in an agricultural area since a series of crops are sequentially grown over time on the same land. In crop rotation systems, crop mimics such as shattercane are subjected to diverse agronomic practices and are affected by alterations in fundamental crop management practices, i.e., tillage, fertilization, irrigation regimes becoming less adaptable and competitive [121]. In addition, crop rotation is accompanied by the rotation of herbicides with different modes of action delaying the selection of herbicide-resistant populations [122]. The importance of crop rotation for the management of shattercane and weedy sunflower was highlighted in the case studies by Werle et al. [63] and Presotto et al. [30], respectively. Diversifying the corn-soybean rotation with cool-season crops such as winter wheat (Triticum aestivum L.) and canola (Brassica napus L.) resulted in significantly lower weedy sunflower infestation in the study by Anderson [123] especially under no-till conditions. Growing a cover crop before the establishment of the main cash crop is another cultural practice that can be used for shattercane and weedy sunflower suppression. In the study by Whalen et al. [124] where shattercane was one of the dominant weeds in a soybean field, a cover crop mixture of cereal rye (Secale cereale L.) and hairy vetch (Vicia villosa Roth) resulted in 83% lower weed biomass; weed suppression increased when the use of cover crops was combined with the application of pre-emergence herbicides with soil residual activity. Sunn hemp (Crotolaria juncea L.) is a cover crop with aggressive growth recently reported to have suppressed weedy sunflower emergence and growth in the subsequent cash crop [125]. Intercropping, narrow row spacing, increased seeding rates, fertilization, and irrigation management should also be investigated for the suppression of shattercane and weedy sunflower. There is evidence that such practices contribute to weed management in summer field crops where shattercane and weedy sunflower are troublesome weeds [126][127][128][129][130]. The selection of competitive hybrids and cultivars was also reported to suppress shattercane in maize and weedy sunflowers in summer legumes such as cowpea [28,64]. In addition, the biological cycle of a particular crop genotype may result in no flowering overlap between the crop and its weedy relatives. Therefore, hybrid and cultivar selection may be an option to prevent crop-weed gene flow in sorghum and sunflower. The same is noted for manipulations in crop sowing dates [3,119].
The preparation of a firm seedbed, the use of germinable crop seed, sowing date and sowing depth selection are also cultural practices ensuring optimal crop growth and can lead to the suppression of noxious weeds such as shattercane and weedy sunflower [117]. False seedbed is another cultural, non-chemical, practice recommended for the control of shattercane and weedy sunflower in a great variety of summer crops including sorghum and sunflower. To apply this practice, the conventional tillage practices used for seedbed preparation are not followed by crop establishment. On the contrary, weeds are left to emerge. At this time, irrigations are encouraged because they stimulate greater weed emergence. After approximately 2 weeks, when the main flush of emergence has passed, weeds are controlled by shallow tillage. Weed control is followed by crop sowing [131]. If shattercane and weedy sunflower populations continue to occur, they can be controlled by subsequent cultivations between crop rows [132].

Herbicides and Mechanical Methods
The strong botanical ties between crops and their weedy relatives precludes, in most cases, selective herbicide use to control shattercane in sorghum fields and weedy sunflower in sunflower fields. The selective control of shattercane and weedy sunflower is possible only when "Inzen" sorghum and "Clearfield" sunflower are treated with ALS-inhibiting herbicides. However, crop-wild gene flow is very likely to result in the spread of herbicideresistant hybrids in the field [30,63]. In any case, herbicide application is more preferable to be carried out before crop sowing under the concept of stale seedbed. Stale seedbed includes the same actions as false seedbed apart from the weed control method. In stale seedbeds, weed control is carried out by the application of a non-selective herbicide [131]. Both glyphosate and pelargonic acid, a natural contact type non-selective herbicide, have been recently reported to provide sufficient control of annual weeds in summer crops [133].
There are more selective herbicide options in crops which are not genetically related to shattercane and weedy sunflower. However, herbicides with different modes of action should be rotated or applied in mixtures to avoid the development of herbicide-resistant populations [118]. As for mechanical methods, cultivation between crop rows can effectively control both species [134,135]. Mechanical operations may need to be repeated; a general recommendation is to increase the number of interrow cultivations to increase the efficacy of mechanical weed control [126]. There is also evidence that multiple mowing operations between crop rows can also provide solutions in shattercane control [136]. The same author denoted that mowing can be effectively combined with herbicide application. Such practices should also be tested against weedy sunflower.

Conclusions
Shattercane and weedy sunflower are two examples of CWRs that have become troublesome weeds in agriculture. Key weedy characteristics such as early seed shattering and seed dormancy play an important role in their success as agricultural weeds. Both species are very competitive to their closely related domesticated crops. Moreover, they can cause severe yield losses in a wide variety of summer field crops. Both species are widely reported as important agricultural weeds in the United States and have invaded various agricultural areas in Europe. Resistance to herbicides was confirmed in both shattercane and weedy sunflower populations. Crop rotation, false seedbed, cover crops, and competitive crop genotypes are valuable cultural practices for suppressing both species.
In addition, preventative measures should be also adopted to avoid their spread to new agricultural land. The development of effective weed management strategies is also essential to prevent hybridization between sorghum, sunflower and their wild relatives and mitigate its consequences.