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2017-Diversidad y Domesticación de La Papa PDF
2017-Diversidad y Domesticación de La Papa PDF
Edited by Esther van der Knaap, University of Georgia, and accepted by Editorial Board Member June B. Nasrallah October 5, 2017 (received for review August
21, 2017)
Cultivated potatoes (Solanum tuberosum L.), domesticated from adopted into the global diet and is the third most important food
wild Solanum species native to the Andes of southern Peru, possess crop for direct human consumption (faostat3.fao.org), providing
a diverse gene pool representing more than 100 tuber-bearing rela- food security in Asia and South America (9, 10).
tives (Solanum section Petota). A diversity panel of wild species, The adaptability of potato to diverse growing conditions stems
landraces, and cultivars was sequenced to assess genetic variation from a large germplasm base encompassing distinct cultivated
within tuber-bearing Solanum and the impact of domestication on groups and over 100 tuber-bearing relatives (Solanum section Petota)
genome diversity and identify key loci selected for cultivation in (11), with distribution ranging from the southwestern United States
North and South America. Sequence diversity of diploid and tetra- to southern Chile (12–14). Potato was domesticated in the Andean
ploid S. tuberosum exceeded any crop resequencing study to date, in highlands (15), an arid region 3,000–4,500 m above sea level char-
part due to expanded wild introgressions following polyploidy that acterized by cold temperatures, saline soils, and high solar radiation.
captured alleles outside of their geographic origin. We identified Rather than an aboveground reproductive structure, the organ of
2,622 genes as under selection, with only 14–16% shared by North selection was an underground tuber highly effective at nutrient
American and Andean cultivars, showing that a limited gene set storage; potato ranks second only to soybean in protein produced
drove early improvement of cultivated potato, while adaptation of per acre among the major crops (16) and ranks first in both energy
upland (S. tuberosum group Andigena) and lowland (S. tuberosum (5,600 kcal/m3) and protein production (150 g/m3) per unit water
PLANT BIOLOGY
groups Chilotanum and Tuberosum) populations targeted distinct (17); a single potato provides 50% of the recommended daily
loci. Signatures of selection were uncovered in genes controlling allowance of vitamin C, compared with 0% for rice and wheat,
carbohydrate metabolism, glycoalkaloid biosynthesis, the shikimate 21% of potassium, 12% of fiber, and balanced protein (18).
pathway, the cell cycle, and circadian rhythm. Reduced sexual fertil- The historic importance and versatility of potato for providing
ity that accompanied the shift to asexual reproduction in cultivars nutrition in diverse environments make its continued improvement
was reflected by signatures of selection in genes regulating pollen a priority to meet global food demands. In an era of genomics-
development/gametogenesis. Exploration of haplotype diversity at enabled breeding, evaluating the genetic diversity of tuber-bearing
potato’s maturity locus (StCDF1) revealed introgression of truncated
alleles from wild species, particularly S. microdontum in long-day– Significance
adapted cultivars. This study uncovers a historic role of wild Solanum
species in the diversification of long-day–adapted tetraploid pota- Worldwide, potato is the third most important crop grown for
toes, showing that extant natural populations represent an essential direct human consumption, but breeders have struggled to
source of untapped adaptive potential. produce new varieties that outperform those released over a
century ago, as evidenced by the most widely grown North
potato | diversity | domestication | introgression | adaptation American cultivar (Russet Burbank) released in 1876. Despite its
importance, potato genetic diversity at the whole-genome
Fig. 1. (A) Phenotypic diversity within wild species, cultivated landraces, and cultivars through domestication, improvement, and modern breeding efforts.
Exemplar species, landraces, and elite North American cultivars are shown that highlight tuber size, shape, and pigmentation diversity. (B) Phylogeny and
population structure of the samples in the domestication panel. The phylogenetic tree is based Nei’s genetic distances calculated from 687,172 fourfold-
degenerate sites from conserved potato genes. Population structure is based on 50,000 genome-wide SNPs. The optimal number of subpopulations (K = 5)
included wild outgroups (purple), wild Solanum relatives (green), a wild subgroup diverging from the cultivated lineage after most other species (gold),
Andean landraces (teal), and S. tuberosum group Tuberosum (navy).
Solanum species and the impacts of human selection is critical for American species sexually compatible with S. tuberosum, excluding
effective germplasm utilization (19). Potato’s domestication altered taxa of hybrid origin. Landraces included 10 diploids (primitive
the regulation of carbohydrate biosynthesis and transport (20, 21) groups Phureja and Stenotomum) and 10 autotetraploids (eight in
and antinutritional glycoalkaloid content (22, 23). Locating targets group Andigena and two in group Chilotanum) with habitats
of selection in critical pathways informs breeding strategies to ranging from equatorial Colombia to southern Chile. Cultivars
control variance of key agricultural traits. This study highlights the represented North American varieties (group Tuberosum) derived
genome diversity of potato and its progenitors, reporting the from Chilean landraces (group Chilotanum) and released over the
greatest levels of genetic variation observed in any crop diversity last 150 y. Although some taxonomic treatments collapse Andean
study to date. We present evidence for a role of wild Solanum S. tuberosum groups Andigena (4x), Phureja (2x), and Stenotomum
species in the evolution of a long-day–adapted S. tuberosum sub- (2x) (24, 25), we invoke the penultimate nomenclature (26) that
specific group and report signatures of selection in genes control- distinguishes ploidy, referring to these as “Andean landraces”
ling both established domestication traits, such as glycoalkaloid (groups Andigena, Phureja, and Stenotomum) for comparison with
biosynthesis and carbohydrate metabolism, and comparatively cultivars (group Tuberosum) and their Chilean landrace progeni-
unexplored potato traits such as circadian rhythm, the shikimate tors (group Chilotanum).
pathway, cell cycling/endoreduplication, and sexual fertility. Sequence and structural variants in the form of SNPs and copy
number variation (CNV) were identified by aligning sequences
Results and Discussion to the S. tuberosum group Phureja DM v4.04 reference genome
Genome Variation and Conservation in Solanum Section Petota. A panel (27). Genome conservation was ascertained from CNV, using a
of 67 genotypes was used to capture a broad extent of genome var- maximum 10% deletion threshold in the respective wild, land-
iation in cultivated potato and its progenitors, including 20 wild race, and cultivar groups to identify 390 Mb of the cultivated
diploid species, 20 South American landraces (groups Andigena, genome (53.5%) containing 63% of genes as conserved among
Phureja, Stenotomum, and Chilotanum) representing locally adapted sexually compatible potato species. High rates of CNV within
primitive selections, 23 North American cultivars (group Tuberosum) individuals and across the panel (Fig. 2A and Dataset S2) ex-
from modern (post-1850) breeding programs, and four outgroups panded previous reports of a structurally heterogeneous genome
(Fig. 1, Fig. S2, and Dataset S1). Wild accessions represented South landscape containing many dispensable loci (Fig. 2B and Fig. S3)
wild species, landraces, and cultivars using SNPs from the conserved
genome. Cultivated potato harbored striking levels of diversity: πC =
20 0.0105 (cultivars), πL = 0.0097 (landraces), and πC+L = 0.0111 (all S.
tuberosum), exceeding estimates from previous crop-resequencing
studies (Fig. 2C) (31–35) and overturning historic assumptions of
10 low founder diversity. Despite having lower heterozygosity than their
tetraploid counterparts (Fig. 2D), diploid potato landraces (πL-2x =
0.0087) exhibited greater diversity than maize landraces (33), up-
holding theories that abundant genome diversity predated poly-
ploidization (27). The similar genome diversities of the combined S.
Landraces & Cultivars Wild Species OG tuberosum lineages and wild Solanum [πW/πC+L = 1.101 (1.188 cod-
ing sequence, CDS)] is remarkable, given that the former represent
Nucleotide Diversity (10-3)
B 0 C 12.5
geographic subgroups of a single cultivated species compared with
Wild
the 20 distinct species representing wild diversity. Potato autotetra-
10.0
Cultivar ploids, containing four homologous chromosomes that undergo
Landrace (4x) tetravalent pairing (36), more than doubled the heterozygosity of
7.5 Landrace (2x) diploid landraces (Fig. 2D) with mean heterozygous nucleotide fre-
quency increasing from 1.05% in diploids to 2.73% in tetraploid
5.0 cultivars (maximum 3.04%). Extensive allele sharing was confirmed
PLANT BIOLOGY
in CDS of wild species, landraces, and North American cultivars,
2.5 with 73% of wild alleles from 20 species extant in cultivated varieties
1000
(53% including rare alleles) (Fig. S4A), suggesting that hybridization
0
with wild populations could have contributed to the heterozygosity
Gene Count
3.0
2000 primary populations: wild species, Andean landraces (groups
Phureja, Stenotomum, and Andigena), and long-day–maturing
2.5
genotypes including group Chilotanum landraces and cultivar de-
scendants. Three Peruvian species (S. medians, S. megistacrolobum,
2.0
and S. raphanifolium) demonstrated substructure within the wild
group, being the wild species closest to the cultivated lineage, while
1.5
outgroup accessions formed a basal wild subgroup. Crop-species
1.0
admixture was asymmetric, with few examples of cultivated alleles
3000 in wild species and frequent evidence of wild introgression into
tetraploid landraces and cultivars (Fig. 1B and Fig. S5). The phy-
logeny resolved tetraploid group Andigena, Chilotanum, and
0.0 0.5 1.0 1.5 2.0 2.5 Tuberosum as more basal to the cultivated lineage than diploids
Est. Copies Per (Fig. 1B and Fig. S5), a surprising result given that potatoes were
Monoploid Genome domesticated as diploids, and extant diploids are more primitive
(37). Genetic distances between cultivated tetraploids and wild
Fig. 2. Genome diversity in tuber-bearing Solanum species. (A) Fraction of species were indeed lower than their diploid progenitors (Fig. S4B)
annotated potato genes affected by duplication (blue), heterozygous deletion due to unequal wild introgression; nine landrace diploids had no
(light red), or homozygous deletion (red) across landraces, cultivars, tuber- evidence of admixture, and the tenth (PI195204) was a mis-
bearing wild-species relatives, and outgroups (OG). (B) Heatmap of gene con- identified wild-crop hybrid, while 9 of 10 landrace tetraploids and
servation across tuber-bearing Solanum genotypes on chromosome 9. Genes
numerous cultivars harbored wild introgression. High rates of wild
are ordered along the chromosome y axis, and the x axis contains samples
organized into panels (separated by thin black lines) containing (Left to Right)
allele sharing and heterozygosity in tetraploids, combined with
20 landraces, 23 cultivars, 20 tuber-bearing wild species relatives, and four
evidence of greater admixture, suggest that autopolyploidy in the
outgroups. (C) Comparison of nucleotide diversity (π) in domesticated germ- cultivated potato lineage altered the dynamics of wild species in-
plasm (cultivars diploid landraces, and tetraploid landraces) and wild relatives teractions, resulting in the diversification of the cultivated gene
for major crop species. Color-coding is shown in the key. Species diversity es- pool by the influx of novel wild alleles.
timates were obtained from existing resequencing studies: cucumber (35),
tomato (35), watermelon (31), rice (32), maize (33), and soybean (34). (D) Het- Wild Solanum Introgression in the Cultivated Lineage. High rates of
erozygous nucleotide frequency within potato outgroups, wild species rela- unreduced (2n) gametes in diploid potatoes reduce barriers to
tives, diploid landraces, tetraploid landraces, and cultivars. interploidy gene flow, helping explain the frequency of wild alleles
landrace (4x) raploids able to tuberize under 16-h days in southern Chile, and
20 landrace (2x) later in Europe and North America, enabling global cultivation at
nonequatorial latitudes. Kloosterman et al. (38) demonstrated that
10
naturally occurring alleles of StCDF1 (positive regulator of tuber-
0 ization via CONSTANS) harbor transposable element (TE)-
induced structural variants resulting in truncated StCDF1 proteins
i
cM / Mb
potato diversification but may have introduced the adaptive 0.10
variants enabling S. tuberosum cultivation in Europe and North 0
FST
0
America. Characterizing a broader set of StCDF1 alleles is re- 0.70 6
quired as reports of this locus as a major yield QTL in Tuber- 0.60
osum populations lacking the TE-induced variant (StCDF1.2) 0.50
0.40 3
support a functional impact of the wild alleles. Discovery of alleles 0.30
impacting StCDF1 protein structure beyond those previously 0.20
0.10
reported shows that disruption of the predominant equatorial 0 0
short-day haplotype has occurred repeatedly by TE-induced 00 10
10 20
20 30
30 40
40 50
50
(StCDF1.2) and non–TE-induced mutations and was intro-
duced into Andean populations from multiple sources following
B Position (Mb)
domestication, which may have enabled tuberization outside their core
earliest geographic range.
confident
Genes Under Selection in Cultivated Potato. Allele frequencies were putative
used to scan the potato genome for gene-selection signatures based
on population metrics comparing North American cultivars against Fig. 4. Genome-wide selection signatures on potato chromosome 6.
(A) Chromosome-wide FST estimates (left axis) from 20-kb sliding window
wild species (cultivar selected) and South American Andean
analysis (5-kb step size) comparing Andean landraces (teal) and S. tuberosum
landraces against wild species (landrace selected). Selected genes group Tuberosum (navy) to wild Solanum; plotted with chromosomal recom-
were ranked under three stringency cutoffs: putative, confident, bination rate in centimorgan/Mb (orange; right axis) based on a diploid bi-
and core, based on scoring in the top 5% (putative), 2% (confi- parental population (111). Red lines indicate top 1% and 5% cutoffs for FST
dent), or 1% (core) values for FST estimates in adjacent genomic window estimates. (B) Locations of genes under putative, confident, and core
windows (20 kb) and at least one per-locus selection metric selective pressure in Andean landraces (teal), S. tuberosum group Tuberosum
(Tajima’s D, relative nucleotide diversity, maximum single-variant (navy), or both groups (domestication candidates; green).
allele frequency difference) within the gene. This approach iden-
tified 2,622 (6.7%) putatively selected genes in cultivated potato,
841 (2.1%) confidently selected genes, and 315 genes (0.8%) under circadian rhythms of wild species, landraces, and cultivars using
core selection (Fig. 4, Fig. S9, and Dataset S7). Domestication delayed fluorescence (Fig. 5 A and B) (44), including wild and
PLANT BIOLOGY
candidates were regarded as genes under selection in both land- cultivated tomato checks to validate our results (43), and observed
races and cultivars, impacting performance regardless of hemi- correlation of period length and latitude of origin (R2 = 0.31) only
sphere or local adaptation. These accounted for only 14.4–16.3% for wild potatoes (Dataset S8). In contrast to their tomato relatives,
of selected loci across all confidence thresholds, evidence that potato landraces and cultivars have maintained similar short pe-
highland Andigena and lowland Tuberosum populations achieved riods independent of latitude (Fig. 5B and Fig. S10), although
agricultural performance by distinct selection strategies, relying similar weakening of clock oscillation was observed (Fig. 5B).
more on regional adaptation than on conserved developmental Correlated period length and latitude have been observed in sev-
processes. Signatures of selection between groups Tuberosum and eral plant species (43, 45, 46); longer circadian periods delay daily
Andigena (Dataset S7) were comparatively weak, lacking strong peaks in gene expression, potentially enhancing growth under
evidence of loci approaching fixation of distinct alleles. longer days by extending the expression of genes controlling
A range of molecular functions, including regulation of gene growth processes (43, 47). However, in monkey flower, correlation
expression, was enriched in genes under selection (Dataset S7). of latitude and period length is observed in annual but not pe-
Tomato domestication involved modification of transcriptional rennial species (48), indicating that modes of reproduction may
networks (39), and transcription factors were enriched in potato influence clock adaptation. As potato shifted to rely on below-
genes with signatures of selection (152 genes, χ2 test, P ≤ 0.005). ground asexual structures for annual regrowth, distinct metabolic
Potato domestication gave rise to enlarged tubers with a con- or developmental processes associated with tuberization and dor-
comitant increase in leaf carbon fixation and transport, tuber- mancy could have selected against changes in the circadian period,
specific reduction of harmful glycoalkaloids, adaptation to a unlike tomato. However, strong selection signatures at regulatory
long-day photoperiod, and reduced sexual fertility. Signatures of loci of the circadian pathway (Fig. 5C) imply that, despite con-
selection associated with key structural and regulatory genes in- servation of a shorter period, potatoes have retuned metabolic or
volved in the cell cycle, circadian rhythm, carbohydrate metabo- physiological responses to the circadian clock.
lism, endoreduplication, glycoalkaloid biosynthesis, shikimate Cell cycle and endoreduplication. Endoreduplication is a deviation from
biosynthesis, and pollen development provide insights into the the standard cell cycle wherein cells forgo cytokinesis, undergoing
biological processes and molecular mechanisms by which ancient successive rounds of DNA replication, increasing ploidy and nuclear
farmers and modern breeders reshaped pathways critical to size. This frequently coincides with increased cellular volume and
agronomic traits. specialized cellular functions such as nutrient storage, as observed for
Circadian rhythm. The plant circadian clock regulates growth, me- maize endosperm (49) and tomato pericarp (50). Considerable
tabolism, and stress responses (40). Clock variation is adaptive, endoreduplication has been observed within potato tubers: DNA
enhancing performance of domesticated species by fine-tuning content as high as 16C (16 times the haploid genome) has been
expression and physiological responses to match fluctuation in observed in cv. Superior and 64C in S. candolleanum, the putative
their environments (41, 42). Migration of domesticated tomato diploid precursor to domestication (51). This, and observations that
(Solanum lycopersicum) from the equator to higher latitudes co- tuber enlargement is primarily due to cell expansion rather than di-
incided with deceleration of its clock, extending the circadian vision (52), suggests that endoreduplication may benefit the tuber’s
period (43). As with tomato, potato domestication preceded mi- function as a sink/storage organ by allowing greater cell expansion
gration to different latitudes with longer summer days. Strong and increasing the potential for starch biosynthesis and deposition.
selection signatures were identified in genes regulating potato Given that endoreduplication has the capacity to increase sink organ
circadian rhythm, including REVEILLE 6 (RVE6) and EARLY size (53), selection of endoreduplication-promoting alleles during
FLOWERING 4 (ELF4) homologs (Dataset S7). We measured domestication and improvement may contribute to differences in wild
D E
B F G
Fig. 5. Circadian rhythms and pollen development phenotypes in wild species, landraces, and cultivars of potato. (A) Example of delayed fluorescence (DF)
traces of one potato wild species and landrace. Data are from one representative experiment; values are the average ± SEM of five (wild) or six (landrace)
plants. (B) Circadian period length and latitude of origin of potato populations. The origin of modern cultivated lines was determined as the location in which
the line was initially bred. Circadian rhythms were measured using delayed fluorescence. Values are the average ± SEM of 2–11 plants from at least two
independent experiments. (C) Simplified model of the photoperiod control of tuberization in potato. Elements in white display signatures of selection. Black
lines represent transcriptional regulation; blue lines represent posttranslational regulation. (D–G) Pollen grains stained with actetocarmine of S. infundi-
buliforme PI 472894 at 10× (D) and 40× (E) magnification and S. tuberosum group Tuberosum cv Superior at 10× (F) and 40× (G) magnification; viable pollen
grains stain red, and nonviable pollen grains are unstained.
and cultivated tuber size (Fig. 1A). We observed selection of 18 genes between wild and cultivated populations (58, 59). This may also be
regulating cell cycle and endoreduplication (Dataset S9), including the case for CCS5B, which is preferentially expressed in developing
the cell-cycle switch 52 gene (CCS52B), showing signatures of se- tissues such as immature tubers (60) and fruit (61), with endor-
lection in both landraces and cultivars. CCS52B homologs are in- eduplication resulting from perturbations in other cell-cycle genes
volved in the shift from mitotic to endoreduplication cycles; when CCS5B is overexpressed. Estimates of endoreduplication in
Arabidopsis CCS52B-overexpressing lines displayed >50% reduction potato tubers have been limited by its recalcitrance to routine flow
in nonendopolyploid root cells (54), whereas tobacco BY-2 cells cytometry protocols; new methodology may improve our un-
overexpressing CCS52B showed a sevenfold increase in cells
with >2C DNA content (55). Selected genes also included two ho- derstanding of the process and genes that regulate it.
mologs of KAKTUS and two cyclins (CYCD3;2 and CYCA3;4), which Sexual reproduction and pollen development. The low sexual fertility
regulate the transition to endoreduplication during organ develop- of cultivated potato is a common hurdle to breeding new culti-
ment (56, 57). While the 13 additional selected cell-cycle genes do vars, as reliance on asexual propagation minimizes the need for
not control endoreduplication, they may have been selected for other sexual fitness. Pollen from wild species and cultivars typically
processes, such as altering the rate of cell division, rather than ex- show wide differences in the frequency of aborted pollen grains
pansion during early organ development, as is the case of the tomato (Fig. 5 D–G). A comparison of cultivars with wild species iden-
fw2.2 domestication locus, which accounts for ∼30% of size variance tified 11 genes controlling aspects of pollen development with
PLANT BIOLOGY
key transcriptional regulator of GAME genes encoding enzymes in (84–87), and both landraces and cultivars have selection signa-
the SGA-specific pathway (Fig. 6, shaded red) (72). Allelic di- tures within the SNF1-related kinase (SnRK1) protein complex.
versity within GAME9 showed broad diversification in wild species. The plant SnRK1 complex directly regulates SPS (88), is required
Squalene Synthase
(SQS)
Glycoalkaloid Metabolism 9 (GAME9)
Ste
Sterol side-chain reductase (SSR2)
(7)-Sterol-C5(6)-Desaturase (C5-SD)
(7)
Fig. 6. Selection impacts within the glycoalkaloid biosynthetic pathway. Plant mevalonate pathway [modified from figure 1 in Ginzberg et al. (69) with permission
from Springer] with branches into terpenoid, lanosterol, steroidal glycoalkaloid (SGA-specific pathway shaded in red), brassinosteroid, and phytosterol biosynthesis.
Red arrows show pathways directly regulated by SQS and GAME9. Blue arrows show pathways controlled indirectly via GAME9 regulation of enzymes guiding
substrates into the SGA-specific pathway.
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