Domestication of “ancestral” cotton in Hainan dates back to 3,000 years ago

When vast cotton fields in Korla, Xinjiang entered their flowering period, scientists were captivated by a single cotton plant that remained unyielding to blossom. This particular wild cotton, originating from Yacheng, Hainan, boasts an extremely ancient genetic “lineage”. Scientists thus embarked on a series of studies, reconstructing its “lost” history from two hundreds of thousands of years ago in the evolution of allotetraploid cotton: around 200,000 years ago, a cotton seed originating from the west coast of Central America drifted westward until it landed on Hainan Island in China. There, it took root, sprouted, and propagated over millennia until about 2,000-3,000 years ago, the ancestors of Hainan Island discovered its descendants and began to domesticate tetraploid cotton.

On January 30, scientists from Zhejiang University published an article titled “Gossypium purpurascens genome provides insight into the origin and domestication of upland cotton” in the Journal of Advanced Research, analyzing the evolutionary status of indigenous upland cotton from Hainan, the semi-wild cotton species G. purpurascens, at the genomic level. It explores the origin and historical significance of G. purpurascens, reveals the role of structural variations (SVs) in the domestication and improvement of upland cotton, and discovers that China is one of the earliest countries to domesticate and cultivate tetraploid cotton.

In 2019, YAN Youfa, then general manager of Xinjiang Yan Seed Company, collected a cotton plant in the wild in Yacheng, Hainan. He later brought it to Korla for use in parent heterosis breeding experiments. While other cotton plants were blossoming, it remained dormant. Puzzled by its behavior, cotton farmers in Korla, accustomed to the predictability of upland cotton or island cotton varieties, sought the expertise of Professor ZHANG Tianzhen’s team from Zhejiang University.

“It is truly a wild cotton plant,” said Professor GUAN Xueying, a member of the research team. “Many wild cotton plants are photoperiod sensitive, with flowering times regulated by the duration of daylight. When they are planted in the north, they may fail to flower.” This trait, impacting cotton quantity and quality, has been bred out of commercially grown varieties worldwide, rendering them insensitive to photoperiod and more adaptable to large-scale cultivation and harvesting.

For ZHANG Tianzhen, an expert in crop genetics and breeding, wild germplasms are an endless treasure trove. On the one hand, they shed light on the reproduction and domestication history of crops on Earth. On the other hand, with the continuous development of breeding technology, various genetic information preserved in wild crops will be further explored. Scientists can cultivate crops that better meet human expectations through various precise breeding methods. Therefore, given its potential value in cotton planting and textile production in China, the cotton research team named this cotton sample “HPF17” and conducted whole-genome sequencing on it. Based on existing resequencing data of upland cotton genomes and 11 tetraploid cotton genomes, the researchers found that the Hainan Island native wild cotton (HIC) represented by HPF17 belongs to a more primitive race of upland cotton’s wild lineage known as G. purpurascens.

In the mountainous regions of China’s Hainan, Guangdong and Guangxi, one may occasionally encounter wild cotton plants that grow naturally. In the last century, British botanists classified these indigenous cotton plants as G. purpurascens, representing a distinct species within the lineage of semi-wild upland cotton.

ZHANG Tianzhen briefly outlined the global cultivation history of cotton: The tetraploid upland cotton (Gossypium hirsutum L.) traces its origin to Central America. Over time, through rigorous artificial selection in the southern United States, this perennial wild species evolved into the cultivated upland cotton or American cotton. By the mid-18th century, it had been disseminated and extensively cultivated worldwide. Early cotton cultivation in China primarily revolved around the diploid cotton species Asian cotton (Gossypium arboreum L.), originating in South Asia. The large-scale cultivation of tetraploid cotton varieties after the year of 1949 also stemmed from the global proliferation of American cotton. Hence, tetraploid cotton, domesticated in the Americas, is labeled as New World cotton, while diploid Asian and African cotton, cultivated for millennia in India, China, and Africa, is termed Old World cotton.

Hainan Island native wild cotton and its fibers and seeds.

Nevertheless, historical records indicate that thousands of years ago, the Li ancestors on Hainan Island already mastered the art of weaving using cotton fibers, utilizing a distinctive indigenous cotton variety known as HIC. However, the arrival of these indigenous G. purpurascens plants in China and their evolutionary trajectory within the broader context of upland cotton evolution remain scientifically unverified. Through comprehensive whole-genome sequencing, ZHANG Tianzhen’s team successfully confirmed the ancient lineage of HIC, establishing it as a direct descendant of the tetraploid upland cotton originating in Central America about 200,000 years ago. “Our research suggests that it diverged from the tetraploid upland cotton of Central American origin as early as 200,000 years ago,” noted ZHANG Tianzhen.

The intriguing question arises: How did cotton seeds from 200,000 years ago find their way to Hainan Island, China? The research team posits that they likely traversed the Pacific Ocean currents, gradually drifting westward from the western shores of Central America to the islands of the South China Sea, including Hainan Island. Two lines of evidence support this hypothesis. Firstly, the distribution patterns of ocean currents align closely with the presence of representative wild allotetraploid cotton on Pacific islands. Several new species of allotetraploid cotton have been identified on this route. Secondly, the robust salt tolerance of these cotton plants enables them to endure prolonged immersion in saltwater, surviving for over six months.

This study illuminates a “forgotten” chapter in the evolutionary history of tetraploid upland cotton. “The genesis of modern cultivated upland cotton varieties may entail multiple origins and undergo distinct domestication events in each respective place of origin,” remarked ZHANG Tianzhen.

Hainan Island boasts an ancient history of cotton cultivation that stretches back well before the planting of G. arboreum in the mainland of China. Yazhou cloth is inscribed on the World Intangible Cultural Heritage list. The ancient book named “Book of Documents” dating to the Spring and Autumn Period ∼ 3,000 years ago records, “Foreigners on the island wear (cotton) cloth for covering; they can weave baskets and cloth.” According to archaeological work in the Changsha Mawangdui, Hunan Province, samples of cotton-spun Yazhou cloth were found (193 BCE). This shows that since the Western Han Dynasty, people have taken fine cotton cloth out of Yazhou.

As far back as the Spring and Autumn Period and the Warring States Period, the Li people of Hainan already mastered the intricate art of utilizing cotton fibers for weaving. However, amidst this historical backdrop, one contentious question lingered: what cotton was planted and used for cloth weaving in Hainan at that time? Was it kapok, HIC, or Island cotton? For generations, this question remained unanswered, shrouded in mystery. Yet, a breakthrough emerged with the advent of the manually-operated cotton ginning machine—a contraption designed to extract seeds from cotton fibers.

In the laboratory of ZHANG Tianzhen’s research team, researchers diligently fed cotton bolls into the ginning machine, day in and day out, extracting fibers for analysis. “The manual extraction of fibers from seeds proved exceedingly laborious, marking the initial hurdle encountered in the evolution of ancient cotton spinning technology,” remarked CHENG Yu, the lead author of the study. Indeed, the cotton ginning machine stood as a relic of ancient ingenuity, with HUANG Daopo, hailed as the “forebearer of cotton,” having learned cotton spinning techniques from the Li people of Yazhou, before promoting the local ginning machine to Shanghai’s Songjiang, thereby catalyzing advancements in cotton spinning technology.

Through meticulous examination of various cotton seed fibers, the research team concluded that only the fibrous strands of G. purpurascens necessitated processing by the ginning machine. “The short fibers of kapok prove unsuitable for weaving, while HIC and Island cotton boast fibers readily separable without mechanical intervention,” said the research team. Thus, it was the distinctive characteristics of G. purpurascens seeds that fueled the invention of the cotton ginning machine.

The research team proposed that approximately 2000-3000 years ago, G. purpurascens had already undergone rudimentary domestication and cultivation on Hainan Island, finding utility in the creation of “Yazhou cloth.” Remarkably, this predates the domestication and cultivation of American cotton, prior to the era of Columbus. “Sanya (Yazhou) may well represent one of the earliest locales for the domestication and cultivation of upland cotton, positioning China as among the pioneers in the domestication of tetraploid cotton,” said ZHANG Tianzhen. Hence, alongside Central America, Sanya (Yazhou) emerges as a probable cradle of upland cotton’s domestication and cultivation.

ZHANG Tianzhen underscored the pivotal role of SVs in plant evolution, domestication, and genetic diversity. Notably, the research team uncovered a plethora of chromosomal SVs across various stages of upland cotton domestication, with 59 SVs pertaining to yield and fiber quality, closely intertwined with upland cotton’s domestication and enhancement. This finding highlights the indispensable role of SVs in crop domestication and improvement. Moreover, a myriad of SVs and QTLs unique to G. purpurascens, as identified in this study, not only enriches our understanding of the origin and evolution of G. purpurascens but also furnishes functional genes crucial for cotton breeding endeavors in China.