How the banana became a virgin

banana-virgin

Bananas are virgins.

Or better-said, edible bananas are virgins. They are sterile and reproduce by making clones of themselves.

Despite being sterile, bananas plants produce (seedless) fruits. This happens without prior fertilization of the ovule via a process called parthenocarpy, literally translating to “virgin fruit”.

So, what happened to bananas? How did they end up with such a screwed sex life? Why are they sterile? In other words: How did the bananas become virgins?

A bit less sex: from wild to edible diploid banana

To answer this question, we have to go back to the origin of the banana (and this blog): to Indonesia. The bananas we know today all originate from Musa acuminata, a wild, spindly banana plant native to the South East Asian islands that make up modern-day Indonesia, Malaysia and Papua New Guinea.

Wild bananas produce tiny fruits filled with hard, inedible seeds and little fruit flesh.  The plants are diploid, that is, they have two copies of each chromosome – just like humans.

banana-morphologySome 6500 years ago, people on the Indonesian archipelago realized that the fruit flesh of Musa was rather tasty. They started selecting Musa plants that produced fruits with more yellow tasty flesh and less seeds. This first step in banana domestication happened independently on many of the thirteen thousand Indonesian islands, resulting in the development of distinct subspecies of Musa acuminata.

When people moved from one island to another, they brought so-far isolated banana subspecies into contact. Occasionally, two subspecies would spontaneously hybridize. To the early banana farmer’s great delight, some of the diploid hybrid bananas produced less seed and more delicious fruit flesh. On the downside, the hybrids had also lost a great deal of their sexual potency. However, bananas can easily be propagated from suckering shoots and the hybrid’s partial impotence did not dull the banana farmer’s joy about its rich fruit flesh.

No more sex: from diploid hybrid to modern triploid bananas

Although the genetically identical progeny remained sterile, banana hybrids could be widely propagated on many of the Indonesian islands. New banana cultivars arose through spontaneous somatic mutations and subsequent selection and propagation by early banana farmers.

Eventually, the banana evolved into its present maiden-like parthenocarpic state after another hybridization event. Through a phenomenon called meiotic restitution, the partially sterile hybrids mated to form triploid bananas (e.g. carrying three copies of each chromosome) with large, seedless fruits of an unheard-of sweetness.

Early banana farmers deliberately selected and propagated the sweet-tasting, parthenocarpic banana hybrids. And because the hybridizations happened many times and among different subspecies on the Indonesian archipelago, we can still find the biggest variety of tastes and shapes of different banana cultivars in Indonesia today.

Tracing back the origin of edible bananas

origin-and-migration-of-aa-cultivars

Origins and migrations of the main triploid subgroups. Plain arrows indicate long-term prehistoric migrations of triploid cvs to Africa and Pacific islands. Gray dotted arrows indicate (i) the migrations of Mlali AAcv subgroup, which is not found in ISEA today, to mainland southeast Asia, where it contributed to AAA Cavendish, then to India, where it met M. balbisiana to give AAB Pome; and (ii) migrations of the Mlali subgroup to the East African coast. Black dotted arrows indicate the route of M. balbisiana from south China to NG over Taiwan and the Philippines. (from: Perrier et al. 2011. PNAS)

A few years ago, a group of scientists used molecular markers to trace back the origin of popular banana cultivars like Cavendish, Gros Michel and the East-African Highland Banana among the existent banana cultivars and landraces. Cultivars that are related to each other through somatic mutations belong to the same subgroup. The scientists succeeded in narrowing down the origin of Cavendish to the Mlali and Khai banana subgroups.  They also resolved the origins of staple crops like plantains and East African Highland Bananas. The East African Highland Bananas are staple crops in Uganda, Rwanda, Kenia and Burundi. After their arrival on the African continent, they underwent further hybridizations – leading to a secondary center of banana diversity in East Africa. Plantains, on the other hand, emerged from hybridization with a different banana species (Musa balbisiana), resulting in a so-called interspecies hybrid. Plantains are popular cooking bananas and staple crops in South America and West Africa.

Banana breeding: the challenges in the absence of sexual reproduction

Banana breeding is a job for the patient. The complicated hybrid genomes and the sterility of edible banana cultivars make it almost impossible to breed new banana cultivars with improved traits such as pathogen resistance or higher yield.

Nevertheless, some brave breeders, scattered in around 12 banana breeding programs around the world, go through the painful process of crossing triploid banana cultivars with improved diploids by hand-pollinating them, searching the pulp of an entire banana bunch for the occasional seed that may form and rescuing the embryo out of that seed to reconstitute a new, hopefully banana with hopefully improved traits like higher yield or better resistance to pests and pathogens. At the National Agricultural Research Organization (NARO) in Uganda, scientist bred an East African Highland Banana with resistance to both the devastating Bacterial wilt and Black Sigatoka diseases.

Other scientists try to pinpoint the genes that cause parthenocarpy and sterility in edible bananas. Solving the genetic riddle behind the banana’s sterility would open doors to successful and less laborious banana breeding and provide many opportunities for preserving our favorite fruit.

 

Original articles:

Perrier, X. et al. 2011. Multidisciplinary perspectives on banana (Musa spp.) domestication. PNAS, 108(28):11311-11318.

Perrier, X., Bakry, F., Carreel, F., Jenny, C., Horry, J.P., Lebot, V. and Hippolyte, I. 2009. Combining biological approaches to shed light on the evolution of edible bananas. Ethnobotany Research and Applications 7:199-216.

Sardos J, et al. 2016. A Genome-Wide Association Study on the Seedless Phenotype in Banana (Musa spp.) Reveals the Potential of a Selected Panel to Detect Candidate Genes in a Vegetatively Propagated Crop. PLOS ONE 11(5): e0154448.

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