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I. Wild Taxa of Cassava Manihot Species

I. Wild Taxa of Cassava Manihot Species

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CASSAVA, M. esculenta Crantz, GENETIC RESOURCES



181



species are typically alogamous plants. However, in cultivated cassava a shift toward autogamous plants has occurred. Nassar and O’Hair (1985) attributed this to

the monoclonal system of cultivation and domestication history. Observations of

frequent hybridization of the wild species and the cultigen and between wild

species suggest weak barriers in the genus (Nassar, 1980a). This is probably due

to the polyploid origin on the genus level.



B. DETERMINATION OF WILD Manihot SPECIES LOCALITIES

WITH EMPHASIS ON PROBABLE ORIGIN

From May to July 1975, I collected seeds of the wild species of Manihot in

northeastern Brazil in three states: Pernambuco, Ceará, and Bahia. the geographical distribution of the Manihot species was studied by Rogers and Appan (1973).

Manihot specimens collected by the expedition of Reading University and deposited at IPA herbarium, Recife, were also examined. Table I lists the wild species

of Manihot that were collected from different localities of northeastern Brazil. It

is apparent that western Pernambuco and central Bahia had the greatest variability in Manihot. It should be noted that certain species reported by the Reading University expedition occur in some localities from which they no longer can be collected (e.g., specimens of M. glaziovii collected about 12 km west of Ibimirim,

PE). Unfortunately, it was found that vegetation in that place had been cleared and

the land cultivated by mamona. Unlike most Manihot species, M. glaziovii grows

in large numbers and not as sporadic plants. Extinction of some wild Manihot

species from their natural habitats may be due to another factor: The majority of

these species are poisonous to grazing animals because of the presence of HCN.



Table I

Wild Species of Manihot Collected from Different Localities

in Northeastern Brazil

Species



Locality



M. caerulescens Pohl

M. heptaphylla Ule

M. cichotoma Ule

M. catingae Ule

M. brachyandra Pax et Hoffmann

M. maracasensis Ule

M. epruinosa Pax et Hoffmann

M. glaziovii Mueller

M. jacobinensis Mueller

M. quinquefolia Pohl



Aparipina, PE

Seabra, BA

Jequie, BA

Itaberaba, BA

Petrolina, PE

Itambé, BA

Bentecoste, Fortaleza, CE

Arcoverde, Ouricure, Serratatlada, PE

Virtoria da Conquista, BA

Senhor do Bonfim, Juazeiro, BA



182



NAGIB M. A. NASSAR



They are known among people of northeastern Brazil as maniỗoba, i.e., the poisonous cassava. Therefore, many plants are exterminated by farmers.

By studying the geographic distribution of Manihot species provided by Rogers

and Appan (1973) combined with localities determined on my trip, it became possible to create a map of concentration of wild species. It shows that in central Brazil

(southern Goias and eastern Minas Gerais) there are approxiimately 38 wild

species of the 98 recognized. Thus, this region includes a large number of wild

Manihot species and represents the highest diversity of these species. In this region the following species occur:

M. acuminatissima Mueller

M. sparsifolia Pohl

M. pruinosa Pohl

M. alutacea Rogers et Appan

M. divergens Pohl

M. cecropiaefolia Pohl

M. triphylia Pohl

M. pentaphylla Pohl

M. anomala Pohl

M. procumbens Mueller

M. crotalariaeformis Pohl

M. Pusilla Pohl

M. logepetiolata Pohl

M. tomentosa Pohl

M. purpureo-costata Pohl

M. attenuata Mueller

M. orbicularis Pohl

M. tripartita (Sprengel) Mueller

M. pilosa Pohl

M. sagittato-partita Pohl

M. falcata Rogers et Appan

M. quinqueloba Pohl

M. violacea Pohl

M. irwinii Rogers et Appan

M. mossamedensis Taubet

M. fruticulosa (Pax) Rogers et Appan

M. gracilis Pohl

M. warmingii Mueller

M. reptans Pax

M. stipularis Pax

M. oligantha Pax

M. nana Mueller



CASSAVA, M. esculenta Crantz, GENETIC RESOURCES



183



M. stricta Baillon

M. salicifolia Pohl

M. weddelliana Baillon

M. peltata Pohl

M. janiphoides Mueller

M. handroana N. D. Cruz

The second largest center of diversity is southwestern Mexico, which includes

M. pringlei Watson

M. aesculifolia Pohl

M. oaxaca Rogers et Appan

M. rhomboidea Mueller

M. walkarae Croizat

M. divisiae Croizat

M. michaelis McVaugh

M. websterae Rogers et Appan

M. auriculata Mcvaugh

M. rubricaulis I. M. Hohnson

M. chlorosticta Standley et Goldman

M. subspicata Rogers et Appan

M. caudata Greenman

M. angustiloba (Torrey) Mueller

M. tomatophylla Standley

M. foetida Pohl

The third largest center of diversity is northeastern Brazil, which includes

M. zenhtneri Ule

M. surinamensis Rogers et Appan

M. quinquefolia Pohl

M. pseudoglaziovii Pax et Hoffmann

M. maracasensis Ule

M. quinquepartita Huber

M. caerulescens Pohl

M. marajoara Chermont de Miranda

M. tristis Mueller

M. glaziovii Mueller

M. epruinosa Paz et Hoffmann

M. brachyandra Pax et Hoffmann

M. dichotoma Ule

M. leptophylla Pax

M. reniformis Pohl

M. heptaphylla Ule



184



NAGIB M. A. NASSAR



Finally, the fourth largest center of diversity is western South Mato Grosso and

Bolivia. It includes the following species:

M. guaranitica Choda et Hassier

M. pruinosa Pohl

M. jacobinsis Mueller

M. condesata Rogers et Appan

M. xavantinensis Rogers et Appan

M. flemingiana Rogers et Appan

Vavilov (1951) showed that variation in cultivated plants is confined to relatively few restricted areas or centers. In 1920, he set up 6 main geographic centers

for cultivated plants and in 1935 increased the number of centers to about 10. He

assumed that the center of diversity for cassava was in the Brazilian–Bolivian center. Vavilov proposed that centers of diversity are places of origin of cultivated

plants. Since this exposition of the center of diversity in the 1920s, much more information has been gathered and it has become clear that not all centers of diversity represent centers of origin. Harlan (1961) showed that more than one center

of diversity may be formed for a given crop through introgression. This phenomenon explained why in many cases there are centers of diversity for a given crop

far from areas of much diversity of wild relatives. Since Harlan proposed this theory (giving a convincing example of the evolved species of Helianthus) much evidence has supported it. Dobzhansky (1973) stated many conspicuous cases, such

as the formation of species of Iris, Eucalyptus, Liatris, Penstemon, and Tragopogon. Thus, this phenomenon serves as a model for what apparently occurred during the formation of these four centers of diversity of Manihot. Assuming that cassava was domesticated for the first time in one place and then carried by Indians

through immigrations, there could then result an extensive hybridization between

the cultivated species and local wild ones, giving rise to numerous new species

through introgression.

Cassava does not grow wild. The large variation of cassava cultivars due to

maintaining them by vegetative reproduction over hundreds of years makes it difficult to designate definite characteristics for M. esculenta. Thus, it is believed that

this species did not arise by natural selection. Hybrids between some wild species

may have been domesticated and maintained afterwards through vegetative reproduction. Surely if these cultivars were left to sexual reproduction and subjected to natural selection, this would have led to different populations with specific

gene pools depending mainly on local environments. Our assumption is that domestication included some natural hybrids and that the selected plants were maintained by vegetative reproduction for hundreds of years. This assumption is supported by the fact that many experimental crosses and observations led to frequent

hybridity of cultivars of M. esculenta and local wild species (Abraham, 1975;

Bolhuis, 1953; Cruz, 1968; Jennings, 1959; Lanjouw, 1939; Magoon et al., 1966;



CASSAVA, M. esculenta Crantz, GENETIC RESOURCES



185



Nichols, 1947). In this genus, systems of genetic and cytologic barriers are not well

established. Additional support may come from Schmidt’s (1951) statement about

the very rapid response of selection in different wild species to increase starch content in tubers and tuber formation through only a few generations. It seems that

many different wild species have the potential to increase tuber formation and

starch content. I observed two tree species of Manihot (M. epuinosa and M.

brachyandra) frequently grown in dooryards at Goiania with considerable tuber

production. These two species are natives of Bahia. It seems that they were carried by people of this state. Immigration was common during the past 30 years due

to the rapid development of Goias. The assumption that domestication included

hybrids and did not include a certain wild species has been discussed by Rogers

(1963) using the expression “species complexity.”

The place of domestication still needs much discussion. I prefer to use “place

of domestication” and not “center of origin” because it is obvious that this crop

was not brought to existence as a wild species by means of natural selection. Studying the history of ethnological groups in Brazil and their immigrations throws light

on the subject. It is reported that the “Aruak,” who lived in north Amazonia more

than 1000 years ago (Schmidt, 1951), knew cassava and practiced a developed

agriculture. Aruak in the Indian language means “people who eat tubers.” Numerous reports indicate that they cultivated cassava many centuries before the arrival of Columbus. The Aruak were obliged to immigrate in the eleventh century

to Central America, crossing the Caribbean and establishing themselves in the

West Indies. Many reasons were given to explain their immigration, but the most

likely are that they were escaping from enemies or possibly looking for a place

where man does not die. However, the most important reason given was that they

were searching for a better soil to cultivate cassava. However, this immigration coincides with the formation of a center of diversity of Mexico. Cassava carried by

the Aruak to Mexico would be expected to hybridize with local wild species, thus

creating a center of diversity. The fact that the Aruak continued on to Planalto Boliviano and to central Brazil is in agreement with the existence of the two centers

of diversity in these regions. The northeastern Brazilian center of diversity is believed to be the result of immigration of the Tupi-Guarani group.

We must still determine which of these four centers constitutes the primary center of diversity of Manihot. In other words, Manihot as a “biological group” must

have passed their differentiation in a certain region from which species spread to

other regions. Central Brazil, with its enormous number of species of Manihot, is

the primary center. Indeed, this region is an ancient area long available for growth

of the angiosperms. Considering Stebbins (1950) explanations of Vavilov’s interpretation of diversity patterns may be useful here: Vavilov’s concept is an elaboration of Willy’s age-and-area hypothesis (i.e., the longer a given biological entity occupies an area, the more variability of Manihot species), and this area might

constitute its primary center of diversity. This assumption is supported by the fact



186



NAGIB M. A. NASSAR



that species which exhibit the most primitive characteristics are restricted to this

region: M. stipularis Pax, M. pusilla Pohl, M. longipetiolata Pohl, with their dioecious inflorescences, and M. stricta Baillon, M. purpureo-costata Pohl, and M.

salicifolia Pohl, with their nonlobed and sessile leaves.



C. RELATIONSHIPS BETWEEN Manihot SPECIES

According to Rogers and Appan (1973), 98 Manihot species have been recognized. Only 1 species, Manihotoides pauciflora, is known in the closest related

genus, Manihotoides. Several of its attributes are not found in any Manihot

species, including uniflorous inflorescences, which is a primitive characteristic

compared with the multiflowered inflorescence in Manihot, and leaves born at the

apex of short, condensed stems arising from branchlets. Rogers and Appan classified Manihot species into 19 sections, varying from trees in the section Glazioviannae to subshrubs, nearly acaulescent, in the section Stipularis. The species in

this latter section are also characterized by being more dioecious than monoecious,

a condition reversed in all other Manihot species. Other sections, such as Tripartitae and Graciles, are perennial subshrubs with large woody roots; their stems frequently die back to the root crown in response to dry periods or fires.

All Manihot species are native to tropical regions of the New World, particularly Brazil and Mexico. Nassar (1978b) defined four centers of diversity for these

species: Mexico and northeast, central, and southwest Brazil. Microcenters of diversity of these species exist within central Brazil, where large numbers of species

are concentrated in small areas (Ͻ50 km in diameter) (Nassar, 1978b,c,d,e,f,

1979a,b, 1980a,b, 1982, 1984, 1985, 1986). Nassar attributes the formation of

these microcenters to the frequent hybridization between species and the heterogenic topography of their habitats, which help isolate fragmented gene pools that

lead to speciation. Tree-like species, such as M. glaziovii and M. pseudoglaziovii,

are found in northeastern Brazil, whereas short species and subshrubs are found in

central Brazil.

Natural hybridization occurs between wild Manihot species and between these

and cassava (Nassar, 1984, 1989). Barriers within the genus appear to be weak due

to recent evolution of the group. All wild Manihot species examined cytogenetically have a chromosome number of 2n ϭ 36 (Nassar, 1978a) (Table II). Despite

this high chromosome number, Manihot species behave meiotically as diploids.

Therefore, they are believed to be allopolyploids and this seems to have anticipated the emergence of the whole group and is responsible for their rapid speciation and their weak interspecific barriers, leading to interspecific hybridization. An

extremely heterozygous gene pool is thus created, followed by differentiation; this

begins a sequence of hybridization followed by speciation. Nassar (1980a) reported frequent hybridization between M. reptans Pax and m. alutacea Rogers et



CASSAVA, M. esculenta Crantz, GENETIC RESOURCES



187



Table II

Chromosome Number in Wild Manihot Species

Species

M. handroana

M. jolyana

M. tripartita

M. tweedieana

M. humilis

M. pedicellaris

M. gracilis

M. dichotoma

M. giaziovii

M. anomala

M. zehntneria

M. olighanta

M. nana

M. tomentosa



Growth habitat

Shrub

Shrub

Shrub

Shrub

Shrub

Subshrub

Shrub

Subshrub

Subshrub

Tree

Tree

Tree

Shrub

Shrub

Subshrub

Subshrub

Subshrub



n



2n









18









18



18



18

18

18

18

18



36

36

36



36

36

36

36



36



36













Appan in sympatric natural habitats in which their population boundaries overlap. Morphological marker gene leaf color and bract size were used to identify

this interspecific hybridization. The range of M. reptans has expanded during the

past 100 years (Nassar, 1984) and this is attributed to the continuing gene introgression of Manihot species. Introgression of M. reptans with germplasm from

other species allowed its ecotypes to penetrate and colonize areas where M. reptans (pure) had previously been unable to do so. This phenomenon was also noted in other species such as M. cearulescens (Nassar, 1980a). From a plant breeding viewpoint, the value of these hybrids lies in their ability to cross with the

cultigen.

Marker genes lobe shape, the presence of stem nodes, flower disc color, fruit

color, and fruit shape were discovered in controlled crosses between cassava and

wild Manihot species as well as in natural hybrids between cassava and different

species. These genes were used by Nassar to identify hybridization. Interspecific

hybrids of cassava with M. glaziovii, M. pseudoglaziovii, M. aesculifolia, M. pilosa, M. corymbilora, M. dichotoma, M. pohlii, M. neusana, and M. anomala were

obtained by Nassar through controlled crosses, although their frequency was low.

The meiotic behavior of several hybrids (cassava with M. neusana and cassava

with M. pseudoglaziovii) was studied by Nassar (1992), and results indicated low

hybrid fertility between these species and cassava.

Grattapaglia et al. (1986) conducted a biosystematic analysis of wild Manihot



188



NAGIB M. A. NASSAR



species based on soluble seed protein pattern. Nineteen species were analyzed

electrophoretically (Table III). A similarity matrix between species, which considered differences in band density and number, was established (Table IV). Several species were found to be highly similar, for example, M. fruticolosa and M.

pentaphylla and M. pilosa and M. corymbiflora. These results correlate well with

the taximetric analysis made by Rogers and Appan (1973). Manihot pilosa and M.

corymbiflora are the most similar species to cassava. Profile analysis confirmed

the introgression between M. cearulescens and cassava. The electrophoresis of

0.1% of SDS was conducted according to Laemilli (1970). The concentrator gel

containing 5.5% of acrylamide Tris–HCl (pH ϭ 6.8) was prepared and fixed during 12 h in 5% trichloroacetic acid. The bands were colored by Coomassie brilliant blue (0.65%). Every species had its profile revealed in four different gels. The

approximate molecular weights (AMWs) were determined according to Webber

and Osborn (1969).



Table III

Wild Manihot Species and Their Identification Number in the Germplasm Bank

at the Universidade de Brasília



Species



Section



M. esculenta Crantz (var. EAB)

I. (A) Manihot

M. esculenta Crantz (var. RB)

(B) Manihot

M. zehntnieri Ule

II. (C) Heterophyllae

M. grahami Hooker

(D) Heterophyllae

M. pilosa Pohl

(E) Heterophyllae

M. corymbioflora Pax

(F) Heterophyllae

M. pohlii Wawra

(G) Heterophyllae

M. glaziovii Muell

III. (H) Glaziovinae

M. pseudoglaziovii Pax et Hoffmann

(I) Glaziovinae

M. epruinosa Pax et Hoffmann

(J) Glaziovinae

M. brachyandra Pax et Hoffmann

(K) Glaziovinae

M. reptans Pax

IV. (L) Crotalariaeformes

M. alutacea Rogers et Appan

V. (M) Quinquelobae

M. fruticulosa Rogers et Appan

VI. (N) Graciles

M. pentaphylla Pohl

(O) Graciles

M. stipularis Pax

VII. (P) Stipulares

M. salicifolia Pohl

VIII. (Q) Brevipetolatae

M. caerulescens subsp. Caerulescens IX. (R) Caerulescentes

M. caerulescens (no classification)

(S) Caerulescentes

M. caerulescens (no classification)

(T) Caerulescentes

M. leptophylla Pax

X. (U) Peuvianae

M. neuzana Nassar

—. (V) —



Habitat

Brasília (DF)

Brasília (DF)

Goiânia (GO)

Maringá (PR)

São Miguel de Antes (MG)

Sóo Miguel de Antes (MG)

Lenỗúis (BA)

Pentocoste (CE)

Remigio (PB)

Serra Talhada (PE)

Currais Novos (RN)

Corumbá (GO)

Goiás Velho (GO)

Alexânia (GO)

Goiás Velho (GO)

Alexânia (GO)

Xavantina (MT)

Picos (PI)

Morro do Chapéu (BA)

Jequié (BA)

Barra do Corda (MA)

Maringá (PR)



No.

01

02

173

375

601

605

139

221

545

554

524

602

115

162

103

184

195

258

567

269

517

360



No.

herbarium

collection

01

01/a

02

03

04

05

06

08

09

10

11

13

07

10,938

11,755

14



15

16

17

12

18



Table IV

Classification of Bands in Wild Manihot Species According to Approximate Molecular Weight (AMW)a

Section

I

No. AMW

(kDaltons)

81–75

75–66

66–62

62–50

50–37.5

37.5–33

33–30

30–27

27–25

25–24

24–21

21–20

20–18

18–13

No. bands

No. reference

bands

No. total

bands

aFor



II



III



IV



V



VI



VII



VIII



IX



X







A



B



C



D



E



F



G



H



I



J



K



L



M



N



O



P



Q



R



S



T



U



V





2

1

3

5

1

1

2

1



1



1

3

21

15





2

1

4

5

1

1

2

1



1



1

1

20

15





2

1

4

6

2

2

2



1



2

1

2

24

15





2

1

3

6

1

2

2







2

2

3

24

14





2

1

3

6

1

1

2





1





3

20

15





2

1

4

6

1

1

2











3

20

15





2

1

4

6

1



2







1

1

3

21

14





2



3

5

1

2

1





1

1



3

19

15





2

1

4

6

1

2

1





1





2

20

15





2

1

4

6

1



1









1

3

19

15





2

1

3

6

1

2

1



1

1





3

20

15





2

1

3

4

1

3

2





1

1



3

21

15





2

1

3

5

1

1

3





1

1

1

3

20

15





2

1

3

3

1

2

1





1





3

17

14





2

1

3

4

1

2

1





1

1



2

18

14





2



1

4

1

3

3





1





2

18

14





2

1

5

5

1

1

1





1



1

2

20

14





1



1

4

1

1

1











2

11

15





1



1

4

1

1

1











3

12

15





3

1

4

5

1

2

1

1





1

1

2

22

15





2



3

3

1

1

1











3

15

15





2

1

3

4

2

2

1



1

1





3

20

14



36



35



39



38



35



35



35



34



35



34



36



36



35



31



32



32



34



26



27



37



30



34



identification species see Table II.



190



NAGIB M. A. NASSAR



To proceed with the analysis of profiles, 15 bands were selected as references;

their aspects were evaluated in all four profiles obtained for every species (Table

V). They were classified into four categories of intensity: A, absent; B, slightly

visible; C, visible; D, dense band; and E, very dense band. To compare quantitatively the protein patterns, the total values of every band were calculated and

expressed in numbers. The protein profiles varied in band intensity, and 15 bands

were selected as references. The variability of wild Manihot species in morphology, growth habit, and geographic distribution was reflected in the electrophoretic profiles as differences in number and intensity of visible bands

(Table VI).

The two studied varieties of cassava showed a 78% similarity with different

species of the section Glaziovinae. Manihot glaziovii Mueller and M. pseudoglaziovii Pax et Hoff showed a high index of similarity based on electrophoresis

analysis. A high similarity was also found in species of the section Gracilis in

which its level reached 78%. The same high similarity was found in species of the

section Heterophyllae. Within this section, the species M. pilosa and M. corymbiflora showed the highest similarity to the cultivated M. esculenta Crantz, coinsidereding at the same time with morphological affinities between them and cassava.

They are probably part of the complex from which the cultigen had originated

(Nassar, 1978b). The high similarity between species in various sections indicates

their recent speciation and accords with the taxonomic classification. Genetically,

they probably share the same gene pool.



D. GENETIC VARIATION OF WILD Manihot SPECIES

Through the program at the Universidade de Brasília, wild Manihot species

were collected from South and Central America, evaluated, reproduced, and

maintained in a living collection (Nassar, 1986). The description and identification of the wild Manihot species was made according to Rogers and Appand

(1973) and Nassar (1978b). Natural habitats were described, and 30 accessions

of each species were examined for the following characteristics: (i) tuber formation and their protein and hydrocyanic acid (HCN) content—tubers were taken 1 year after planting and analyzed according to the Association of Official

Analytic Chemists (AOAC) methods (1970); (ii) adaptation to various soil

types—chemical analysis of soil was carried out according to Black et al.

(1965); (iii) data regarding adaptation to various habitats were extracted from

records of federal meteorological stations; and (iv) seeds, cuttings, or whole

plants of the collected species were planted in a living collection at the Universidade de Brasília. The collected wild Manihot species were screened rapidly

for tuber formation and growth habit. Results of this screening are given in

Table VII.



Table V

Distribution of Reference Bands According to Density in Studied Wild Manihot Species Profilesa

Section

I



II



III



Reference band

No.AMW



A



B



C



D



E



F



G



H



I



J



01/81

02/75

03/66

04/62

05/50

06/37.5

07/33

08/30

09/27

10/25

11/24

12/21

13/20

14/18

15/13



B

B

C

C

C

C

E

C

C

B

B

D

D

D

D



B

B

C

C

D

D

E

B

C

B

B

D

D

D

D



B

B

C

C

C

C

B

B

C

B

B

B

B

D

D



B

B

C

C

C

C

B

C

C

B

C

B

A

C

C



B

B

C

C

D

C

D

C

C

B

B

C

C

C

C



B

B

C

C

C

C

B

C

C

B

B

B

C

D

C



B

B

C

C

C

C

C

C

C

C

B

C

A

C

C



B

B

C

C

B

C

D

C

B

B

B

C

C

D

D



B

B

C

C

C

C

D

C

B

B

D

C

C

D

C



B

B

C

C

C

C

C

E

D

B

B

C

C

D

D



IV



V



VI



K



L



M



N



B

B

C

C

C

C

C

D

D

B

B

C

C

C

C



B

B

C

C

C

C

B

C

C

C

D

C

C

C

C



B

B

C

C

B

B

B

B

B

B

B

B

B

C

C



B

B

C

C

C

C

D

C

B

B

B

E

E

B

A



Note. Abbreviations used: A, absent band; B, slightly visible band; C, visible band; D, dense band; E, very dense band.

aSee Table III for species identification.



IX



VII



VIII



O



P



Q



R



S



B

B

C

C

B

B

D

C

B

C

B

E

E

B

A



B

B

C

C

B

B

D

B

A

B

B

E

E

B

C



B

B

C

C

C

C

D

C

C

C

C

C

B

D

A



B

B

C

C

B

B

B

C

C

D

C

B

B

B

C



B

B

C

C

B

B

B

C

C

D

C

B

C

B

C



X







T



U



V



B

B

C

C

D

D

C

C

C

C

C

C

C

D

C



B

B

C

C

C

C

D

C

C

B

D

B

B

D

C



B

B

C

C

C

C

D

C

C

C

C

C

A

B

C



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I. Wild Taxa of Cassava Manihot Species

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