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Hemibiotrophs

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Hemibiotrophs are the spectrum of plant pathogens, including bacteria, oomycete and a group of plant pathogenic fungi that keep its host alive while establishing itself within the host tissue, taking up the nutrients with brief biotrophic-like phase.[1][2] It then, in later stages of infection switches to a necrotrophic life-style, where it rampantly kills the host cells, deriving its nutrients from the dead tissues.[3]

This mode of interaction, in which initial biotrophy followed by a switch to necrotrophy, has been observed in the fungal model Magnaporthe oryzae (rice blast fungus) and other pathogens such as many Colletotrichum spp. (often called anthracnose diseases, e.g. Colletotrichum lindemuthianum), Southern corn leaf blight (Bipolaris maydis) and, Zymoseptoria tritici (syn. Mycosphaerella graminicola, leaf blotch of wheat).[4][5][6] Collectively, they represent some of the most destructive plant parasites, causing huge economic losses, threatening global food security.[7]

A spectrum of hemibiotrophic plant pathogens, including the bacterium Pseudomonas syringae, the and the oomycete Phytophthora infestans (potato blight) also exhibit characteristics of both biotrophs and necrotrophs and thus are called as hemibiotrophs, depending on the stages of their life cycle.

Life style

In contrast to biotrophs, hemibiotrophs have dual life-styles. The initial biotrophic life-style of hemibiotrophs causes minimum damage to the plant tissues, while the fungus obtains nutrients from living plant tissues [8] Hemibiotrophic fungi require living plant tissue to survive to complete their life cycle.

Most fungal hemibiotrophs develop haustoria, whereas some produce intracellular hyphae to acquire nutrients from the host cytoplasm.[9][10] However, in the hemibiotrophic life-style the pathogen later breaks down host cell walls through secretion of hydrolytic enzymes and feeds on the released nutrients.[8][11] These hydrolytic enzymes and toxins are synthesized during the later necrotrophic phase. They also produce extracellular hyphae between the host cells to facilitate nutrient assimilation.[8][9] Plant pathogenic fungi produce and secrete many so‐called effector proteins that interact with the host and play an important role in virulence.

The rice blast fungus Magnaporthe oryzae[12] and Colletotrichum species are generally considered to be hemibiotrophs.[8][1][13] Three hemibiotrophic species, Colletotrichum pisicola, C. vignae and C. destructivum belong to the Colletotrichum destructivum complex. Fusarium oxysporum  is the cause of fusarium wilt disease and Moniliophthora roreri, which causes frosty pod rot disease of cacao, are hemibiotrophs that affect many agricultural and floricultural crops worldwide [14][15][16]

In the early stages of infection, the pathogens proliferate asymptomatically in the host by suppressing programmed cell death (PCD) or thwarting host defense responses, but in the later stages of infection they undergo a physiological transition from asymptomatic biotrophic growth to a highly destructive necrotrophic phase. Hemibiotrophic bacteria are known to secrete a range of so-called effector proteins, including transcription factors and others with enzymatic activities, into host cells via the type III secretion system (T3SS)[17] whereupon they suppress PCD and other host defenses.[18][19]

Hemibiotrophy genes

Studies have shown that fungal hemibiotrophic C. lindemuthianum species undergo two distinct phases during invasion in the host. The first phase is the biotrophic phase which involves the generation of intracellular hyphae within intact plant cells. Later, extracellular hyphae tend to cross the cellular boundaries, moving past the plasmodesmata and ramify between host cells—the necrotrophic phase.

The suggestion that these fungi undergo a distinct metabolic switch from biotrophic to necrotrophic growth was boosted by the discovery of a gene that functions between the biotrophic and necrotrophic phases. The gene CLTA1 encodes a GAL4‐like transcriptional activator, which is consistent with a role in reprogramming metabolism. It is clear that all pathogens are obliged to alter metabolic fluxes in numerous ways upon penetration to prepare for proliferation. This is a key postulated attribute of the hemibiotrophs and seems to be a priority subject for study.[4]

Life cycle of hemibiotrophs

The hemibiotrophic life cycle involves an initial biotrophic phase and later a necrotrophic phase.[8][9] Colletotrichum lindemuthianum is a hemibiotrophic fungus on beans (common bean anthracnose).[4][20][21] Conidia then, on the host surface, germinate and differentiate to form a melanized infection structure devoted to mechanical penetration of the epidermal cells.[12][21] After the penetration step, the infection cycle is characterized by two successive phases. In the first phase, lasting 3 to 4 days, the fungus grows biotrophically inside the infected epidermal cells. During this phase, referred to as the biotrophic phase, the appressoria develops into a primary penetration hypha, which is surrounded by the invaginated plant plasma membrane, during this phase the penetrated host cell remains alive with minimum damage. The second phase, which corresponds to the appearance of symptoms, is completed 6 to 8 days after inoculation. During this phase, the necrotrophic phase, the fungus develops secondary hyphae that grow both intracellularly and intercellularly and thus acts as a typical necrotrophic pathogen. During the necrotrophic phase the fungus secretes cell wall-degrading enzymes that break down the host cell wall. After a few days the plant cell membrane disintegrates and ultimately the host cell dies.[12][17] Thereafter the fungus grows as a necrotroph.

Another hemibiotroph is Moniliophthora roreri, which causes frosty pod rot on Theobroma sp. (Cacao).[21] It produces meiospores, via meiosis, from the modified basidium.[21][22] These spores are important as dispersal agents, for infection and survival.[22] Meiospores germinate and produce hyphae made up of haploid cells throughout the biotrophic phase. The necrotrophic phase is thought to start from the formation of dikaryotic hyphae and continues until sporulation on the pod surface.[13][22][23]

References

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  2. ^ Lee, Sang-Jik; Rose, Jocelyn K.C. (June 2010). "Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins". Plant Signaling & Behavior. 5 (6): 769–772. doi:10.4161/psb.5.6.11778. ISSN 1559-2324. PMC 3001586. PMID 20400849.
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  13. ^ a b Latunde-Dada, A. O.; Lucas, J. A. (2007-03-12). "Localized hemibiotrophy in Colletotrichum: cytological and molecular taxonomic similarities among C. destructivum, C. linicola and C. truncatum". Plant Pathology. 56 (3): 437–447. doi:10.1111/j.1365-3059.2007.01576.x. ISSN 0032-0862.
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  17. ^ a b Alfano, James R.; Collmer, Alan (September 2004). "TYPE III SECRETION SYSTEM EFFECTOR PROTEINS: Double Agents in Bacterial Disease and Plant Defense". Annual Review of Phytopathology. 42 (1): 385–414. doi:10.1146/annurev.phyto.42.040103.110731. ISSN 0066-4286. PMID 15283671.
  18. ^ Espinosa, Avelina; Alfano, James R. (November 2004). "Disabling surveillance: bacterial type III secretion system effectors that suppress innate immunity". Cellular Microbiology. 6 (11): 1027–1040. doi:10.1111/j.1462-5822.2004.00452.x. ISSN 1462-5814. PMID 15469432. S2CID 35641145.
  19. ^ Chisholm, Stephen T.; Coaker, Gitta; Day, Brad; Staskawicz, Brian J. (February 2006). "Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response". Cell. 124 (4): 803–814. doi:10.1016/j.cell.2006.02.008. ISSN 0092-8674. PMID 16497589. S2CID 10696351.
  20. ^ Dufresne, Marie; Perfect, Sarah; Pellier, Anne-Laure; Bailey, John A.; Langin, Thierry (September 2000). "A GAL4-like Protein Is Involved in the Switch between Biotrophic and Necrotrophic Phases of the Infection Process of Colletotrichum lindemuthianum on Common Bean". The Plant Cell. 12 (9): 1579–1589. doi:10.1105/tpc.12.9.1579. ISSN 1040-4651. PMC 149071. PMID 11006333.
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  22. ^ a b c Münch, Steffen; Lingner, Ulrike; Floss, Daniela S.; Ludwig, Nancy; Sauer, Norbert; Deising, Holger B. (January 2008). "The hemibiotrophic lifestyle of Colletotrichum species". Journal of Plant Physiology. 165 (1): 41–51. doi:10.1016/j.jplph.2007.06.008. ISSN 0176-1617. PMID 17765357.
  23. ^ Evans, Harry C. (December 2007). "Cacao Diseases—The Trilogy Revisited". Phytopathology. 97 (12): 1640–1643. doi:10.1094/phyto-97-12-1640. ISSN 0031-949X. PMID 18943725.
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