What we know so far and what we can expect next: A molecular investigation of plant parasitism

Ishida, Juliane Karine; Costa, Elaine Cotrim

doi:10.1590/1678-4685-GMB-2024-0051

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Young Latin American Geneticists - Special Issue • Genet. Mol. Biol. 47 (Suppl 1) • 2024 • https://doi.org/10.1590/1678-4685-GMB-2024-0051 linkcopy

What we know so far and what we can expect next: A molecular investigation of plant parasitism

Authorship SCIMAGO INSTITUTIONS RANKINGS

The review explores parasitic plants’ evolutionary success and adaptability, highlighting their widespread occurrence and emphasizing the role of an invasive organ called haustorium in nutrient acquisition from hosts. It discusses the genetic and physiological adaptations that facilitate parasitism, including horizontal gene transfer, and the impact of environmental factors like climate change on these relationships. It addresses the need for further research into parasitic plants’ genomes and interactions with their hosts to better predict environmental changes’ impacts.

Keywords:
Parasitic plant; HGT; haustorium; plastid genome; mitochondrial genome

Authorship

person Juliane Karine Ishida

wrote the manuscript · read and approved the final version

schoolUniversidade Federal de Minas Gerias (UFMG), Instituto de Ciências Biológicas, Departamento de Botânica, Belo Horizonte, MG, Brazil.Universidade Federal de Minas GeriasBrazilBelo Horizonte, MG, BrazilUniversidade Federal de Minas Gerias (UFMG), Instituto de Ciências Biológicas, Departamento de Botânica, Belo Horizonte, MG, Brazil.

0000-0002-0956-7578

person Elaine Cotrim Costa

wrote the manuscript · read and approved the final version

schoolUniversidade Federal do Rio Grande (FURG), Instituto de Ciências Biológicas, Rio Grande do Sul, RS, Brazil.Universidade Federal do Rio GrandeBrazilRio Grande do Sul, RS, BrazilUniversidade Federal do Rio Grande (FURG), Instituto de Ciências Biológicas, Rio Grande do Sul, RS, Brazil.

0000-0001-6625-7595

personSend correspondence to Juliane Karine Ishida. Universidade Federal de Minas Gerias (UFMG), Instituto de Ciências Biológicas, Departamento de Botânica, Av. Antônio Carlos, 6627, Bloco G- 2º andar - Sala G245, 31270-901, Belo Horizonte, MG, Brazil. E-mail:
julianeishida@ufmg.br.

Associate Editor:

Felipe Maraschin

Conflict of Interest

The authors declare that no conflict of interest could be perceived as prejudicial to the impartiality of the reported research.

SCIMAGO INSTITUTIONS RANKINGS

Universidade Federal de Minas Gerias (UFMG), Instituto de Ciências Biológicas, Departamento de Botânica, Belo Horizonte, MG, Brazil.Universidade Federal de Minas GeriasBrazilBelo Horizonte, MG, BrazilUniversidade Federal de Minas Gerias (UFMG), Instituto de Ciências Biológicas, Departamento de Botânica, Belo Horizonte, MG, Brazil.

Universidade Federal do Rio Grande (FURG), Instituto de Ciências Biológicas, Rio Grande do Sul, RS, Brazil.Universidade Federal do Rio GrandeBrazilRio Grande do Sul, RS, BrazilUniversidade Federal do Rio Grande (FURG), Instituto de Ciências Biológicas, Rio Grande do Sul, RS, Brazil.

Figures

Figures (4)

Thumbnail

Figure 1 - Genome size of parasitic plants compared to nonparasitic plants. Only those with fully sequenced and assembled genomes. The arrangement reflects the degree of host dependence. At the top, in green, are the free-living plants, which include Manihot esculenta (Alaba et al., 2014), Arabidopsis thaliana (Lamesch et al., 2012), Ipomoea nil (Hoshino et al., 2016), Mimulus guttatus (Hellsten et al., 2013) and Lindenbergia luchunensis (Xu et al., 2022). In light yellow is the facultative hemiparasite Phtheirospermum japonicum (Cui et al., 2020)- the obligate hemiparasite Striga asiatica (Yoshida et al., 2019) in dark yellow. Holoparasites are depicted in orange/red and include Cuscuta australis (Sun et al., 2018), C. campestris (Vogel et al., 2018), Orobanche cumana (Xu et al., 2022), and Phelipanche aegyptiaca (Xu et al., 2022). Lastly, the endophytic holoparasite Sapria himalayana (Cai et al., 2021) is shown in red, representing the most extreme parasitism.

Thumbnail

Figure 2 - Estimated genome size (C-value) of parasitic plants. The C-values were obtained from Plant DNA C-values Database (Leitch et al., 2019) maintained by Kew Royal Botanic Garden. The prime estimated c-value (in Mbp) from the database was compared with a list of parasitic plant genera (U.S. DEPARTMENT OF AGRICULTURE, 2024). Only families that have a minimum of two genera of parasitic plant species with documented C-values in the database were examined in this analysis. The grey bars represent the range of C-values observed in each group, from the lowest to the largest, while the red bars indicate the average genome size. The dashed line indicates the average genome size of all angiosperm plants recorded in the database. For Santalaceae, the genera included were Rhoiacarpos sp., Santalum sp. and Comandra sp. In Orobanchaceae, the listed genera were Bartsia sp., Bellardia sp., Cistanche sp., Euphrasia spp., Melampyrum spp., Nothobartsia sp., Odontitella sp., Parentucellia sp., Pedicularis spp., Phelipanche spp., Phelypaea spp., Schwalbea sp., Orobanche spp., Pedicularis spp., Odontites ssp. and Rhinanthus spp. Convolvulaceae included Cuscuta spp. Loranthaceae encompassed the genera Alepis sp., Amylotheca sp., Benthamina sp., Decaisnina spp., Dendrophthoe spp., Diplatia spp., Amyema spp., Nuytsia sp., Loranthus spp., Lysiana sp., Macrosolen sp., Ileostylus sp., Muellerina spp., Peraxilla spp., Sogerianthe sp. and Tupeia sp. Finally, Viscaceae comprised Viscum spp. and Arceuthobium sp.

Thumbnail

Figure 3 - Number of protein-coding genes in the genome of parasitic plants compared to nonparasitic plants. Only those with fully sequenced and assembled genomes. The arrangement reflects the degree of host dependence. At the top, in green, are the free-living plants, which include Manihot esculenta (Alaba et al., 2014), Arabidopsis thaliana (Lamesch et al., 2012), Ipomoea nil (Hoshino et al., 2016), Mimulus guttatus (Hellsten et al., 2013) and Lindenbergia luchunensis (Xu et al., 2022). In light yellow, facultative hemiparasite Phtheirospermum japonicum (Cui et al., 2020). The obligate hemiparasite Striga asiatica (Yoshida et al., 2019) in dark yellow. Holoparasites are depicted in orange/red and include Cuscuta australis (Sun et al., 2018), Cuscuta campestris (Vogel et al., 2018), Orobanche cumana (Xu et al., 2022), and Phelipanche aegyptiaca (Xu et al., 2022). Lastly, the endophytic holoparasite Sapria himalayana (Cai et al., 2021) is shown in red, representing the most extreme parasitism.

Thumbnail

Figure 4 - The progression of haustoria formation in P. japonicum (A) Initially, the figure on the left illustrates the root’s anatomical layers without a host, highlighting its independent structure. (B) The prehaustorium phase marks the beginning of haustorial development. (C) This phase transitions into the invading haustorium stage, where the haustorium starts to penetrate the host tissue. (D) The process culminates in the mature haustorium stage, establishing a vascular connection with the host and facilitating nutrient exchange. The diagram labels various anatomical features, including the epidermis (Ep), cortex (Co), endodermis (Ed), vascular system (VS), haustorial hairs (HH), paratracheal parenchyma (PP), procambium-like cells (PL), intrusive cells (IC), tracheary elements (TE), xylem bridge (XB), and plate xylem (PX), to illustrate the complex interactions and transformations involved in haustoria development.

imageFigure 1 - Genome size of parasitic plants compared to nonparasitic plants. Only those with fully sequenced and assembled genomes. The arrangement reflects the degree of host dependence. At the top, in green, are the free-living plants, which include Manihot esculenta (Alaba et al., 2014), Arabidopsis thaliana (Lamesch et al., 2012), Ipomoea nil (Hoshino et al., 2016), Mimulus guttatus (Hellsten et al., 2013) and Lindenbergia luchunensis (Xu et al., 2022). In light yellow is the facultative hemiparasite Phtheirospermum japonicum (Cui et al., 2020)- the obligate hemiparasite Striga asiatica (Yoshida et al., 2019) in dark yellow. Holoparasites are depicted in orange/red and include Cuscuta australis (Sun et al., 2018), C. campestris (Vogel et al., 2018), Orobanche cumana (Xu et al., 2022), and Phelipanche aegyptiaca (Xu et al., 2022). Lastly, the endophytic holoparasite Sapria himalayana (Cai et al., 2021) is shown in red, representing the most extreme parasitism. open_in_new

imageFigure 2 - Estimated genome size (C-value) of parasitic plants. The C-values were obtained from Plant DNA C-values Database (Leitch et al., 2019) maintained by Kew Royal Botanic Garden. The prime estimated c-value (in Mbp) from the database was compared with a list of parasitic plant genera (U.S. DEPARTMENT OF AGRICULTURE, 2024). Only families that have a minimum of two genera of parasitic plant species with documented C-values in the database were examined in this analysis. The grey bars represent the range of C-values observed in each group, from the lowest to the largest, while the red bars indicate the average genome size. The dashed line indicates the average genome size of all angiosperm plants recorded in the database. For Santalaceae, the genera included were Rhoiacarpos sp., Santalum sp. and Comandra sp. In Orobanchaceae, the listed genera were Bartsia sp., Bellardia sp., Cistanche sp., Euphrasia spp., Melampyrum spp., Nothobartsia sp., Odontitella sp., Parentucellia sp., Pedicularis spp., Phelipanche spp., Phelypaea spp., Schwalbea sp., Orobanche spp., Pedicularis spp., Odontites ssp. and Rhinanthus spp. Convolvulaceae included Cuscuta spp. Loranthaceae encompassed the genera Alepis sp., Amylotheca sp., Benthamina sp., Decaisnina spp., Dendrophthoe spp., Diplatia spp., Amyema spp., Nuytsia sp., Loranthus spp., Lysiana sp., Macrosolen sp., Ileostylus sp., Muellerina spp., Peraxilla spp., Sogerianthe sp. and Tupeia sp. Finally, Viscaceae comprised Viscum spp. and Arceuthobium sp. open_in_new

imageFigure 3 - Number of protein-coding genes in the genome of parasitic plants compared to nonparasitic plants. Only those with fully sequenced and assembled genomes. The arrangement reflects the degree of host dependence. At the top, in green, are the free-living plants, which include Manihot esculenta (Alaba et al., 2014), Arabidopsis thaliana (Lamesch et al., 2012), Ipomoea nil (Hoshino et al., 2016), Mimulus guttatus (Hellsten et al., 2013) and Lindenbergia luchunensis (Xu et al., 2022). In light yellow, facultative hemiparasite Phtheirospermum japonicum (Cui et al., 2020). The obligate hemiparasite Striga asiatica (Yoshida et al., 2019) in dark yellow. Holoparasites are depicted in orange/red and include Cuscuta australis (Sun et al., 2018), Cuscuta campestris (Vogel et al., 2018), Orobanche cumana (Xu et al., 2022), and Phelipanche aegyptiaca (Xu et al., 2022). Lastly, the endophytic holoparasite Sapria himalayana (Cai et al., 2021) is shown in red, representing the most extreme parasitism. open_in_new

imageFigure 4 - The progression of haustoria formation in P. japonicum (A) Initially, the figure on the left illustrates the root’s anatomical layers without a host, highlighting its independent structure. (B) The prehaustorium phase marks the beginning of haustorial development. (C) This phase transitions into the invading haustorium stage, where the haustorium starts to penetrate the host tissue. (D) The process culminates in the mature haustorium stage, establishing a vascular connection with the host and facilitating nutrient exchange. The diagram labels various anatomical features, including the epidermis (Ep), cortex (Co), endodermis (Ed), vascular system (VS), haustorial hairs (HH), paratracheal parenchyma (PP), procambium-like cells (PL), intrusive cells (IC), tracheary elements (TE), xylem bridge (XB), and plate xylem (PX), to illustrate the complex interactions and transformations involved in haustoria development. open_in_new

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