Peach Genome Dissected to Provide Insights into Ecological Influences

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The humble peach has been the inspiration for pies, album titles, independent movies, and a fictional woman's baseball team, but is also an important food species, yielding 24.5 million tons globally in 2018.  Like all plant species, their sessile nature makes them a good target for environmental studies because, unlike most animals, they must respond to changes in their environment by adaptation rather than flight.  They have a diverse temperate host range from their origins in southwestern China, being found in temperate and subtropical regions, wet and dry climates, and in harsh environments (high altitudes, severe cold, and drought conditions).  This range suggests that the peach is a good species for studying climate effects on their evolution as illustrated by genetic changes, particularly in view of the climate change the globe has been experiencing for the past ~40 years that is expected to continue.

An international group of researchers* recently reported the results of their taking this suggestion, in a paper entitled "Genomic analyses provide insights into peach local adaptation and responses to climate change" in the journal Genome Research.  The basis for the study was 263 diverse accessions that consisted of 52 wild relatives and 211 landraces ("a domesticated, locally adapted, traditional variety of a species of animal or plant that has developed over time, through adaptation to its natural and cultural environment of agriculture and pastoralism, and due to isolation from other populations of the species").  The 263 peach accessions could be divided into seven major groups:  YG (Yun-gui plateau), NW (Northwest China), NP (North Plain China), YT (Yangtze River Middle and Backward), NE (Northeast China), TB (Tibet plateau), and ST (South China Subtropical) groups.  Placing their genome assay results in context, these researchers reported on the effects of glaciation, which had caused a sharp decline of effective population size during the two largest Pleistocene glaciations:  the Xixiabangma glaciation (that occurred 1.17–0.8 million years ago, mya) and the Naynayxungla glaciation (occurring 0.78–0.50 mya); there was also a smaller decline in population size during the "last glacial maximum" (LGM) about 20,000 years ago.  Also reported was a slight expansion of peach populations from the Tibetan plateau (TB) after the Naynayxungla glaciation about 300,000 years ago.

In total, 342.7 Gb of paired-end sequences were assayed, with a median depth of 5.3-fold corresponding to 91.7% of a reference peach genome ("Lovell"); the peach genome is relatively small (227.4 Mb) compared with other fruit species (e.g., apple, 650 Mb; and strawberry, 805 Mb).  These sequencing studies resulted in the identification of 4,611,842 single-nucleotide polymorphisms (SNPs), with 1,931,310 residing in introns (∼11.33%) and another 848,638 (∼4.98%) in protein-coding exons.  These researches also identified 1,049,266 small insertions and deletions (indels) (< 6 bp) and 106,388 larger structural variations (>30 bp).  These variations were used as genetic markers for mapping through time genomic changes and crossbreeding between the different geographically defined groups.  The results of these genetic analyses showed a pattern of extensive admixture and possible gene flow among landrace groups.

Genetic analyses identified specific loci involved in adaptation to local conditions.  These include a total of 2092 genomic regions found for all seven groups (comprising 19.1 Mb, ∼8.4%) and "189, 387, 301, 235, 280, 339, and 378 regions for the YG, NW, NP, YT, NE, TB, and ST groups, respectively."  These loci were termed candidate selection regions (CSRs) by these researchers, and together harbored 3742 genes, corresponding to 396, 966, 635, 403, 573, 743, and 680 genes for the YG, NW, NP, YT, NE, TB, and ST groups.  In addition, some of these genes were shared among different groups, "suggesting the unique adaptive patterns for each group and that different climates may shape distinct genomic regions" according to the authors.  Assessment of these genes identified several related to response to different types of stimuli and stress that were overrepresented; included were temperature, radiation, salt, DNA damage, osmotic, toxin, and biotic stimulus.  These results suggested to these researchers that these genes were involved in adaptive evolution in response to these stresses.

Turning to specific forms of environmental stress, the researchers found that peach specimens from high-salt soils in northwestern China were enriched for two cation/H+ exchanger family genes.  Additional genes found from to be enriched in these specimens were genes encoding proteins having a leucine-rich repeat (LRR) domain, comprising 121 of 612 members (∼19.8%).  These researchers noted that such genes were "considered to be one of the most important domains involved in plant resistance."  Pattern recognition receptor (PPR) proteins, which "form one of the largest protein families in land plants that are related to environmental responses" and are present with 286 members in the peach genome, were found in 79 (∼27.6%) of the identified candidate selection regions (CSRs).

Specific genetic characteristics were reported for certain groups.  For the YG group (which is found on the Yun-gui plateau (Southwest China), a low-latitude (∼23.3–26.6° N) and high-altitude (∼2000 m) region with acidic soil (pH 4.5∼5.5)), genes (107) related to "metal ion (including potassium, iron, and zinc) binding and transport, cell membrane function, and response to toxins" were found to be overrepresented.  These scientists found that expression of a phenotype encoded by these genes would be "consistent with functions in overcoming cation deficiency and aluminum toxicity that are common in acidic soils."  For the YT group, characterized by high temperature and high humidity areas in middle and lower regions of the Yangtze river, the researchers found "high enrichments of the LRR domain (24) genes," as well as other genes related to stress responses (40 genes), in comparison to other groups.

The paper also reported on genes correlated with altitude and adaptations to altitude.

These include 2755 association SNPs, involving 2408 genes, of which 1670 association SNPs were unique, and ∼51.9% of the associations were shared across different types of environmental variable (EVs), which suggested to them that different EVs may shape the same genomic regions.  These "hotspots" were located at "the top and bottom of Chromosome 2," wherein the top was enriched with genes encoding NBS-LRR proteins and the bottom was highly enriched with genes associated with responses to a series of stresses, as well as at the top of Chromosome 4, which was "highly enriched with genes associated encoding LRR domain-containing proteins."  Overall, a "total of 75 genomic loci associated with more than five EVs were identified and these loci were highly enriched with genes in stress-related pathways, such as plant–pathogen interaction, MAPK signaling pathway, response to stress, and defense response."

Related to specific stresses, the researchers found that "genes involved in ion transport were highly enriched in those associated with soil pH . . ., as soil pH affects absorption of metal ions in plants."  Also enriched were genes associated with "programmed cell death (PCD), innate immune response, plant–pathogen interaction, and DNA repair," as well as "secondary metabolism, including flavonoid metabolic process, jasmonic acid (JA) biosynthesis, and plant hormone signal transduction."  These researchers also identified "temperature-associated SNPs [including] 10 association hotspots on Chromosomes 1, 2, 3, 4, 5, 6, and 7 for more than eight EVs related to temperature and altitude."  These findings were significant, according to the authors, because "[t]olerance to low temperature in winter is a major factor that restricts the spread of peach to extremely cold regions."  One particular SNP identified in this way was "located in the gene PpAHP5" which is part of a gene cluster encoding six histidine phosphotransfer proteins (AHP); these have been "reported to be involved in mediating cold signaling" and was found to be "up-regulated by cold," and cold-resistant cultivars expressed the gene at higher levels than cold-sensitive ones.  Similarly, the researchers reported precipitation-related "hotspots"; one of these showed enrichment of several stress response related genes.

Of economic importance, the level of fruit produced by cultivars adapted to different environmental conditions was determined, and the researchers reported finding differential expression of genes resulting in higher soluble sugar content.  Environmental factors associated with this phenotype include aridity, high diurnal temperature variation, and long sunshine duration, according to these scientists, leading them to conclude that "higher soluble sugar content in accessions from northwestern China represents an adaptive trait driven by the local drought environment."

Other phenotypes include fruit flesh color, which the researchers found "strong geographic patterns, with ∼80% of yellow-fleshed peach landraces originating from northwestern China" and to be related to carotenoid metabolism (particularly overexpression of genes associated with carotenoid synthesis and loss-of-function mutations leading to carotenoid accumulation).  Studies of genetic variants associated with high altitude (Tibet) adapted cultivars were also reported, including specific patterns of gene expression, enrichment and loss (339 genomic regions, harboring 743 genes for high altitude cultivars, including ones involved in flavonoid production and UVB protection, and morphological changes in stomata thought to be involved in resistance to high-altitude hypoxia).

The depth of genetic information and environmental factor correlations (much more extensive than set forth in this synopsis) led these researcher to conclude:

In summary, this study provides new insights into peach adaptation to its habitat and how climate has shaped the genome of a perennial tree through natural selection.  These results also provide a new resource for studies of peach evolutionary biology and breeding, especially with regard to enhancing stress resistance.

* Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences; National Horticulture Germplasm Resources Center, Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences; Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture & Forestry Sciences, Huazhong Agricultural University;  Agricultural Genome Institute at Shenzhen, Chinese Academy of Agricultural Sciences;  IRTA–Centre de Recerca en Agrigenòmica (CSIC-IRTA-UAB-UB); Boyce Thompson Institute for Plant Research, Cornell University; U.S. Department of Agriculture– Agricultural Research Service, Robert W. Holley Center for Agriculture and Health

DISCLAIMER: Because of the generality of this update, the information provided herein may not be applicable in all situations and should not be acted upon without specific legal advice based on particular situations.

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