**4. Botanical class and carbon metabolism pathway**

**3.3. Botanical genera**

144 Herbicide Resistance in Weeds and Crops

*Raphanus*.

from Heap [8].

group of importance, following *Amaranthus*.

The botanical genera with resistant species in the reference countries are shown in **Figure 10**. In Australia, *Lolium* was the predominant genus in number of resistant weed species; in Canada and the United States, *Amaranthus* is the most important one; in France, there is no predominant genus with the most cases of resistant weed biotypes being *Avena, Amaranthus, Lolium, Setaria*, and *Echinochloa* similar in importance (**Figure 10**). In Australia, *Raphanus, Bromus, Hordeum, Avena*, and *Sisymbrium* are the second most important group of genera with resistant weed biotypes; in Canada, *Setaria* and *Avena* are also in the second group. In the United States, a great number of botanical genera with resistant weed biotypes occur, but *Echinochloa, Conyza, Poa, Setaria, Kochia, Ambrosia*, and *Lolium* may be highlighted in a second

In Brazil, 19 genera with resistant biotypes are reported (**Figure 11**), where *Amaranthus, Conyza*, and *Bidens* are the most important ones, followed by *Digitaria, Lolium*, and *Echinochloa* in the second group. A third group includes *Sagittaria, Euphorbia, Eleusine, Cyperus*, and

**Figure 10.** Wordcloud for the occurrence of weed resistance as a function of botanical genus in the reference countries. The scale of the font represents the importance of the genus compared to the others in the same figure. Source: adapted As mentioned earlier, plant taxonomy is not static, and from time to time some adaptations are proposed to plant nomenclature by different authors [17], trying to adjust plant classification under the light of new evolutionary evidences or simply aiming to rearrange previous taxonomic trees. Angiosperms are, in a free definition, plants with flowers whose seeds are protected in fruits [13, 18]. Along the history, different plant classification systems were proposed, which can be roughly divided into three groups: (1) artificial systems, based on superficial features; (2) natural systems, based on form relationships; and (3) phylogenetic systems, based on evolutionary and genetic relationships [18].

The artificial systems are very old, based usually on a single character, and have been used as example by Theophrastus (370 285 BC) and Linnaeus (1707 1778 AD); natural systems were based on a set of botanical characters, being used in the eighteenth and nineteenth centuries; examples are the classification systems of Jussieu and Bentham & Hooker [19]. Among the phylogenetic systems, Cronquist [20], later reviewed in 1988 [21], is one of the most used, and it divides flowering plants into two classes: (1) Magnoliopsida (dicotyledons, dicots) and (2) Liliopsida (monocotyledons, monocots). With no intention to start a war among plant taxonomists and considering the division into these two classes is the most common in the weed science, we grouped resistant plant species into dicots and monocots (**Figure 12** and **Figure 13**).

Australia has 34 dicot species with resistant biotypes, while 54 monocot weed species had at least one resistant biotype (**Figure 12**). Monocot species were also the majority in France, where 20 dicots and 26 monocots had at least one resistant biotype. In the northern region of the American continent, dicots predominated among the species with resistant biotypes; 59 and 108 dicots contrasted with 31 and 87 monocots, in Canada and the United States, respectively (**Figure 12**).

**Figure 12.** Occurrence of weed resistance as a function of botanical class in the reference countries. Source: adapted from Heap [8].

When weed species with resistant biotypes were grouped in the reference countries by the carbon metabolism (C3, C4, intermediary/hybrid/unknown) (**Figure 13**), there was a clear predominance of C3 species over C4 in the number of plant species with resistant biotypes for all countries; 75, 49, 115, and 25 weed species with at least one biotype resistant to herbicides were C3, while only 5, 31, 71, and 14 were C4, respectively, for Australia, Canada, the United States, and France (**Figure 13**).

Plant species with carbon metabolism by the C4 cycle, in evolutionary terms are derived from the C3 cycle [22]; furthermore, although it is generally claimed that C4 plant species are most widely distributed in warmer and dry environments compared to C3 plants, this is not remarkable since C4 plants evolved to optimize carbon fixation in low-C environments, and not essentially to resist to water stresses as usually believed [23]. In fact, C4 plants may be equally or even more sensitive to water stress than C3 species, in spite of the greater water use efficiency of C4 plants [24].

In Brazil, where the majority of the arable territory is located in warm climates with mild winters, there were no significant differences in the proportion of dicots (22) and monocots (20) with resistant biotypes (**Figure 14**). In North America (Canada and the United States), dicot

**Figure 13.** Occurrence of weed resistance as a function of carbon metabolism pathway in the reference countries. Source: adapted from Heap [8].

When weed species with resistant biotypes were grouped in the reference countries by the carbon metabolism (C3, C4, intermediary/hybrid/unknown) (**Figure 13**), there was a clear predominance of C3 species over C4 in the number of plant species with resistant biotypes for all countries; 75, 49, 115, and 25 weed species with at least one biotype resistant to herbicides were C3, while only 5, 31, 71, and 14 were C4, respectively, for Australia, Canada, the United States, and France (**Figure 13**). Plant species with carbon metabolism by the C4 cycle, in evolutionary terms are derived from the C3 cycle [22]; furthermore, although it is generally claimed that C4 plant species are most widely distributed in warmer and dry environments compared to C3 plants, this is not remarkable since C4 plants evolved to optimize carbon fixation in low-C environments, and not essentially to resist to water stresses as usually believed [23]. In fact, C4 plants may be equally or even more sensitive to water stress than C3 species, in spite of the greater water

**Figure 12.** Occurrence of weed resistance as a function of botanical class in the reference countries. Source: adapted from

In Brazil, where the majority of the arable territory is located in warm climates with mild winters, there were no significant differences in the proportion of dicots (22) and monocots (20) with resistant biotypes (**Figure 14**). In North America (Canada and the United States), dicot

use efficiency of C4 plants [24].

Heap [8].

146 Herbicide Resistance in Weeds and Crops

weed species with resistant biotypes predominated, while in France and Australia, monocots tended to predominate (**Figure 13**).

Dicot species may have advantages over monocots. With no intention to differentiate these two groups of plants, some traits from each group may be highlighted: first, the vascular bundle of dicots may allow flow of higher volumes of sap to and from leaves, as well as up and down into the plant compared to monocots; second, the stronger vascular bundle could allow dicots to resist stronger water potentials, which could be advantageous in both rich and scarce water environments; third, the two cotyledons could allow for higher photosynthesis rates to dicots, which would depend less on the seed stored energy to form its initial leaf area, increasing their chance of survival [22]. These facts could help explain why dicots were superior to monocots in Canada and the United States. On the other side, bulliform cells which are present in many monocots—not only in grasses—may help avoiding stress by excessive light incidence in low latitude environments [23, 24], which could turn it into a big advantage for some groups of monocots in tropical agriculture.

**Figure 14.** Occurrence of weed resistance as a function of botanical class in Brazil. Source: adapted from Heap [8].

There was also no difference in the proportion of plants as a function of the carbon metabolism pathway (**Figure 15**). Ehleringer and Monson [23] report that in anthropogenically altered environments, C4 plants are usually not so advantageous over C3. In the reference countries (**Figure 13**), most weed species with resistant biotypes were C3, but in Brazil (**Figure 15**) this difference was not remarkable. By considering this, one may hypothesize that in Brazil most of the arable lands are as intensely explored as consequence of the anthropogenic effect, that it led C4 plants to almost totally lose their superior potential compared to C3 weeds in the same environment.

When the data of angiosperm class is crossed with the data of carbon metabolism pathway (**Figure 16**), visually there appears to be little to no relationship between these factors; but when we apply a *X*<sup>2</sup> test to the data *Ang.Class* x *Carb.Metab*, (*Dic./Mon*. vs. *C3/C4* only), it turns out to be significant at 5% probability for all countries, except the United States (**Figure 16**). This supplies initial evidence that C3 and C4 species with resistant biotypes to herbicides may not be equally distributed into dicots and monocots. In Brazil (**Figure 16**), most dicots are C3

**Figure 15.** Occurrence of weed resistance as a function of carbon metabolism pathway in Brazil. Source: adapted from Heap [8].

while most monocots with resistance to herbicides are C4; for Australia and France, C3 species also predominate in the monocot class, while in Canada the proportion of C3 and C4 species with any biotype resistant to herbicides is equivalent (**Figure 16**).

In other words, it appears that the dicot class of angiosperms is significant (four out of four) for presenting a higher number of C3 species with resistant biotypes compared to C4. For monocots, Australia and France presented higher number of C3 species with resistance; in Canada, this relationship was alike, and in Brazil, there were more C4 monocot species with resistance to herbicides than C3. Anyway, the carbon metabolism pathway (**Figure 13** and **Figure 15**) seems to be the most significant compared to the angiosperm class (**Figure 12** and **Figure 14**). Thus, one would expect more cases of C3 weed biotypes with resistance to herbicides in Brazil (**Figure 15**), compared to the reference countries (**Figure 13**), for dicots (**Figure 16**). For monocots, there will be a need for a follow-up to understand if the tendency of majority in C4 species (**Figure 16**) will be maintained, or if it is only a deviation

There was also no difference in the proportion of plants as a function of the carbon metabolism pathway (**Figure 15**). Ehleringer and Monson [23] report that in anthropogenically altered environments, C4 plants are usually not so advantageous over C3. In the reference countries (**Figure 13**), most weed species with resistant biotypes were C3, but in Brazil (**Figure 15**) this difference was not remarkable. By considering this, one may hypothesize that in Brazil most of the arable lands are as intensely explored as consequence of the anthropogenic effect, that it led C4 plants to almost totally lose their superior potential compared to C3 weeds in the

**Figure 14.** Occurrence of weed resistance as a function of botanical class in Brazil. Source: adapted from Heap [8].

When the data of angiosperm class is crossed with the data of carbon metabolism pathway (**Figure 16**), visually there appears to be little to no relationship between these factors; but

out to be significant at 5% probability for all countries, except the United States (**Figure 16**). This supplies initial evidence that C3 and C4 species with resistant biotypes to herbicides may not be equally distributed into dicots and monocots. In Brazil (**Figure 16**), most dicots are C3

**Figure 15.** Occurrence of weed resistance as a function of carbon metabolism pathway in Brazil. Source: adapted from

test to the data *Ang.Class* x *Carb.Metab*, (*Dic./Mon*. vs. *C3/C4* only), it turns

same environment.

148 Herbicide Resistance in Weeds and Crops

when we apply a *X*<sup>2</sup>

Heap [8].


**Figure 16.** Occurrence of weed resistance as a function of botanical class and carbon metabolism pathway. Source: adapted from Heap [8].

from the real tendency which will be corrected by nature in the future. One should consider the probable loss of superiority from C4 plants over C3 as a consequence of the heavy anthropogenic effect in arable fields, as hypothesized by Ghannoum [24].

## **5. Geographical region of origin of families with resistant biotypes**

The **probable** geographical center of origin of the families with resistant biotypes is summarized by the studied country in **Figure 17**. The region of origin for each botanical family is

**Figure 17.** Occurrence of weed resistance as a function of the **probable** geographical region of origin of the genus. Source: adapted from Heap [8].

difficult to be defined, and data is sometimes controversial; thus, **Figure 17** should be interpreted as an approximation as close as possible to the currently available data about the origin of plant families. Families with higher degrees of uncertainties in their origin were grouped, like "Eurasia," which includes Europe and Asia, Eurasia-Africa (Europe, Asia, Africa), and Europe-Africa.

Most botanical families with resistant weed biotypes in Australia were originated in Eurasia and Africa; in Canada, they came from America and Eurasia (and of course Europe); in France, most weeds with resistant biotypes are native from Europe, and some of them could have come from Asia (Eurasia). In the United States, most families are native from the Americas, while about a half of the species with resistant biotypes came from Eurasia (in **Figure 17**, Asia + Eurasia + Europe data).

Summarizing, half or most of the weed species, which presented resistant biotypes in each of the reference countries, seem to be native to their continent (**Figure 17**), and this makes sense since the center of genetic origin of a given botanical group usually (if not always) presents the greatest genetic variation for that species [25]. Thus, the genetic variation which could result in the appearance and consequent selection of resistant biotypes would probably be most easily present in the genetic center of origin of the plant group. In Brazil (**Figure 17**), the same tendency is observed as most of the plants which presented resistant biotypes were most probably native from the Americas.
