Abstract
Since the dawn of agriculture, plant pathogens and pests have been a scourge of humanity. Yet we have come a long way since the Romans attempted to mitigate the effects of plant disease by worshipping and honoring the god Robigus [1]. Books in the Middle Ages by Islamic and European scholars described various plant diseases and even proposed particular disease management strategies [1]. Surprisingly, the causes of plant diseases remained a matter of debate over a long period. It took Henri-Louis Duhamel du Monceau's elegant demonstration in his 1728 “Explication Physique” paper that a “contagious” fungus was responsible for a saffron crocus disease to usher in an era of documented scientific inquiry [2]. Confusion and debate about the exact nature of the causal agents of plant diseases continued until the 19th century, which not only saw the first detailed analyses of plant pathogens but also provided much-needed insight into the mechanisms of plant disease. An example of this is Anton de Bary's demonstration that a “fungus” is a cause, not a consequence, of plant disease [3]. This coming of age of plant pathology was timely. In the 19th century, severe plant disease epidemics hit Europe and caused economic and social upheaval. These epidemics were not only widely covered in the press but also recognized as serious political issues by governments [1], [4]–[6]. Many of the diseases, including late blight of potato, powdery and downy mildew of grapevine, as well as phylloxera, were due to exotic introductions from the Americas and elsewhere. These and subsequent epidemics motivated scientific investigations into crop breeding and plant disease management that developed into modern plant pathology science over the 20th century. Nowadays, our understanding of plant pathogens and the diseases they cause greatly benefits from molecular genetics and genomics. All aspects of plant pathology, from population biology and epidemiology to mechanistic research, are impacted. The polymerase chain reaction (PCR) first enabled access to plant pathogen DNA sequences from historical specimens deposited in herbaria [7]–[9]. Historical records in combination with herbarium specimens have turned out to provide powerful tools for understanding the course of past plant epidemics. Recently, thanks to new developments in DNA sequencing technology, it has become possible to reconstruct the genomes of plant pathogens in herbaria [10], [11]. In this article, we first summarize how whole genome analysis of ancient DNA has been recently used to reconstruct the 19th-century potato-blight epidemic that rapidly spread throughout Europe and triggered the Irish potato famine. We then discuss the exciting prospects offered by the emergence of the discipline of ancient plant pathogen genomics.
Highlights
Nowadays, our understanding of plant pathogens and the diseases they cause greatly benefits from molecular genetics and genomics
The polymerase chain reaction (PCR) first enabled access to plant pathogen DNA sequences from historical specimens deposited in herbaria [7,8,9]
Thanks to new developments in DNA sequencing technology, it has become possible to reconstruct the genomes of plant pathogens in herbaria [10,11]
Summary
DNA retrieved from historic and prehistoric sources such as museum specimens, archaeological finds, and fossil remains is collectively known as ancient DNA (aDNA) [12]. The sequencing of the complete genomes of two archaic hominins (Neanderthals and Denisovans) has opened a window to the past and profoundly changed our views on human origins [16,17,18]. Such a historic perspective is starting to arise for infectious diseases. The complete genome sequences of medieval bacterial pathogens have started to answer questions about the origin and history of infectious human diseases such as bubonic plague and leprosy [20,21,22]. The surprisingly high quality of aDNA in these samples suggests that the millions of dried plant samples that are stored in herbaria throughout the world hold great promise for the future study of past plant epidemics
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