Genome sequence of Striga asiatica provides insight into the evolution of plant parasitism

Authors: YOSHIDA, SATOKO - Riken Institute; KIM, SEUNGILL - Seoul National University; WAFULA, ERIC - Pennsylvania State University; TANSKANEN, JAAKKO - Natural Resources Institute Finland (LUKE); KIM, YONG-MIN - Korea Research Institute Of Bioscience And Biotechnology; Honaas, Loren; YANG, ZHENZHEN - Pennsylvania State University; SPALLEK, THOMAS - Riken Institute; CONN, CAITLIN - University Of Georgia; ICHIHASHI, YASUNORI - Riken Institute; CHEONG, KYEONGCHAE - Seoul National University; CUI, SONGKUI - Riken Institute; DER, JOSHUA - California State University; GUNDLACH, HEIDRUN - Helmholtz Centre; JIAO, YUANNIAN - Chinese Academy Of Sciences; HORI, CHIAKI - Riken Institute; ISHIDA, JULIANE - Riken Institute; KASAHARA, HIROYUKI - Riken Institute; TAKATOSHI, KIBA - Riken Institute; KIM, MYUNG-SHIN - Seoul National University; KOO, NAMJIN - Korean Bioinformation Center (KOBIC); LAOHAVISIT, ANUPHON - Riken Institute; LEE, YONG-HWAN - Seoul National University; LUMBA, SHELLEY - University Of Toronto; MCCOURT, PETER - University Of Toronto; MORTIMER, JENNY - Riken Institute; MUSEMBI MUTUKU, J. - Riken Institute; NOMURA, TAKAHITO - Utsunomiya University; SASAKI-SEKIMOTO, YUKO - Tokyo Institute Of Technology; SETO, YOSHIYA - Tohoku University; WANG, YU - University Of Virginia; WAKATAKE, TAKANORI - Riken Institute; SAKAKIBARA, HITOSHI - Riken Institute; DEMURA, TAKU - Riken Institute; YAMAGUCHI, SHINJIRO - Tohoku University; YONEYAMA, KOICHI - Utsunomiya University; MANABE, RI-ICHIROH - Riken Institute; NELSON, DAVID - University Of Georgia; SCHULMAN, ALAN - Natural Resources Institute Finland (LUKE); TIMKO, MICHAEL - University Of Virginia; DEPAMPHILIS, CLAUDE - Pennsylvania State University; CHOI, DOIL - Seoul National University; SHIRASU, KEN - Riken Institute

Submitted to: Current Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/30/2019
Publication Date: 9/23/2019
Citation: Yoshida, S., Kim, S., Wafula, E., Tanskanen, J., Kim, Y., Honaas, L.A., Yang, Z., Spallek, T., Conn, C., Ichihashi, Y., Cheong, K., Cui, S., Der, J., Gundlach, H., Jiao, Y., Hori, C., Ishida, J.K., Kasahara, H., Takatoshi, K., Kim, M., Koo, N., Laohavisit, A., Lee, Y., Lumba, S., McCourt, P., Mortimer, J.C., Musembi Mutuku, J., Nomura, T., Sasaki-Sekimoto, Y., Seto, Y., Wang, Y., Wakatake, T., Sakakibara, H., Demura, T., Yamaguchi, S., Yoneyama, K., Manabe, R., Nelson, D.C., Schulman, A.H., Timko, M.P., dePamphilis, C.W., Choi, D., Shirasu, K. 2019. Genome sequence of Striga asiatica provides insight into the evolution of plant parasitism. Current Biology. 29(18):3041-3052.e4. https://doi.org/10.1016/j.cub.2019.07.086.
DOI: https://doi.org/10.1016/j.cub.2019.07.086

Interpretive Summary: In this paper we report the genome of Striga asiatica, a parasitic plant in the family Orobanchaceae. It is a serious constraint to agriculture in many nations in Africa and threatens many more outside Africa. In fact, an outbreak of Striga in the Carolinas was the focus of the most costly eradication effort in USDA history. The genome will be an important resource for the research community as it is the first parasitic plant genome. In addition to a resource that can be used to develop control methods for parasitic weeds, it provides a resource to understand the evolution of novel traits. Genome and gene duplication, plus co-option of tissue specific genes (e.g. a pollen gene being copied and used in a new tissue) seem to be a source of novel plant functions and traits. Gene families that have evolved in the host detection process (from karrakin receptors - karrikins are smoke-derived compounds that stimulate germination of many nonparasitic plants) are greatly expanded in Striga, providing a genetic mechanism for the wide host range of this pernicious weed. The attachment organ (haustorium) uses many genes that are specific to other tissues in other plants, especially pollen and roots. We also discovered that the haustorium of Striga seems to use lateral root genes during its development. The methods utilized here represent novel approaches to detecting and characterizing genome level changes that underpin new plant traits.

Technical Abstract: Parasitic plants in the genus Striga, commonly known as witchweeds, cause major crop losses in sub-Saharan Africa and pose a threat to agriculture worldwide. An understanding of Striga parasite biology, which could lead to agricultural solutions, has been hampered by the lack of genome information. Here we report the draft genome sequence of Striga asiatica and the comprehensive transcriptome of Striga hermonthica. We detected a recent whole genome duplication in S. asiatica, which might have enabled the evolution of parasitism and/or adaptation to host plants. Striga seeds germinate in response to host-derived strigolactones (SLs)and then develop a specialized structure, the haustorium, to attach to and penetrate the host root. A family of likely SL receptors has undergone a striking expansion, suggesting a molecular basis for the evolution of broad host range among Striga species. We found that genes involved in lateral root development in nonparasitic model species are coordinately induced during Striga haustorium development, suggesting that a lateral root pathway was coopted during the evolution of the haustorium. In addition, we found evidence for the horizontal transfer of host genes and retrotransposons, indicating genetic flow between S. asiatica and its hosts. Our results provide new insights into parasitism in plants and a key resource for the future development of Striga control strategies.