Puccinia oxalidis Dietel & Ellis (1895): first report controlling oxalis latifolia kunth (Oxalidaceae) in systems of direct planting

The genera Puccinia (Pucciniaceae) includes more than four thousand species of fungi described (Kirk et al. 2008), mostly restricted to one host. The species diversity of Pucciniaceae is greatest in the genera Puccinia and Uromyces (Van der Merwe et al., 2007). The fungus Puccinia oxalidis Dietel & Ellis (1895) (Pucciniaceae), native to the southern part of the United States of America, Mexico, and South America (Šafránková, 2014), has been reported in the southern United States, Australia, China, India, Japan, Central and South America, New Zealand and South Korea (Farr and Rossman 2018; Lee et al., 2019). Puccinia species are pathogens of plants cultivated or not from different families, mainly Asteraceae, Cyperaceae, Fabaceae, Lamiaceae, Liliaceae, Malvaceae, Poaceae, and Oxalidaceae (Marin-Felix et al., 2017; Talhinhas et al., 2019).

Oxalis latifolia Kunth, originally from Mexico (Burger, 1991), a perennial plant with slow growth (Everard et al., 2018) and leaves in long petioles composed of three broad leaflets, is commonly known as “clover” or “sorrel” with asexual reproduction (bulbs). This species has been described as a weed in agricultural crops (Shrestha et al., 2019) and as a host of different rust-causing Puccinia species (Vacacela Ajila et al., 2018).

Fungal plant pathogens are increasingly recognized and studied worldwide for the biological control of invasive weeds (Ireland et al., 2019; Maharjan et al., 2020).

The hypothesis studied is that P. oxalidis can control O. latifolia, reducing or avoiding the use of chemicals to manage this plant in less disturbed systems such as in no-till vegetables. The objective of this work was to describe the occurrence of biological control of O. latifolia by P. oxalidis in no-tillage under straw in the culture of garlic.

The fungus P. oxalidis was observed between August and October 2018 on O. latifolia plants in the experimental area of the Olericulture sector of the Federal University of Jequitinhonha and Mucuri Valleys (UFVJM), municipality of Diamantina, located in the Espinhaço Meridional region, Minas Gerais state, Brazil (18°10'S and 43°30'W; 1387 masl). The local climate is Cwb - dry winter subtropical highland, according to the Köppen classification (Köppen, 1936), with dry winters and rainy summers. The minimum temperature was 15°C, the maximum was 23°C and the rainfall was 67.70 mm. The local soil is classified as Typical Ortic Quartzene Soil, according to the Brazilian Soil Classification System (SiBCS).

Samples of O. latifolia plants were collected and placed in Petri dishes and taken to the phytopathology laboratory of the UFVJM for analysis under a microscope and identification.

The propagation structure of O. latifolia, as resistant bulbs, allows surviving under different temperature and soil conditions and reinfestation by this weed until 140 days under no-tillage (Arianoutsou et al., 2010). In addition, the high number of seeds with rapid germination after stresses, such as the application of the desiccant herbicide for straw formation, may have favored the reinfestation by O. latifolia (Royo-Esnal and López-Fernández, 2010).

The fungus P. oxalidis covered the leaves of O. latifolia under no-tillage with the presence of pustules and urediniospore (Figure 1C and D). The sperm and aecial stages of this fungus were observed and its basidiospores germinated and penetrated the leaves (Guerra et al., 2019) of Oxalis spp. Puccinia oxalidis dinfested and causes rust in O. latifolia with powdered pustules on the abaxial surface of infected leaves (Lee et al., 2019), which quickly become powdery (Versluys, 1977), reducing growth and causing the wilting and death of this plant (Figure 2). The golden yellow color of rust urediniospores of P. oxalidis is due to the carotenoid pigments accumulated in the lipid droplets in its structure (Wang et al., 2019).

Figure 1
Clover (Oxalis latifolia) under no-tillage of the Allium sativum L. culture (A), rust caused by Puccinia oxalidis on the abaxial surface of the clover leaf (B), P. oxalidis pustules under a stereomicroscope (magnifying glass) (C), P. oxalidis urediniospore with circular shape (D).

Figure 2
Stages of infection by Puccinia oxalidis in clover (Oxalis latifolia). Clover leaf without rust infection (A), onset of rust infection (B), rust across the leaf abaxial surface (C), leaf severely infected with symptoms of wilt and necrosis (D).

Puccinia spp. develop better and sporulate on the target plant, without damage to the crops, due to the microclimate of the decomposing straw in no-tillage, controlling different weeds like Fallopia japonica (Ueda et al., 2018). The straw can improve the environment for natural enemies (Trewavas, 2004), like this fungus, due to humidity and mild temperatures while reducing the competition between O. latifolia and garlic plants. The biological control by the fungus P. oxalidis prevented the competition of O. latifolia with garlic plants in no-tillage, even though it was the main weed species at 60 days after the beginning of this culture.

The weed O. latifolia predominated in the plots with no-tillage, but the rust on its leaves, caused by the fungus P. oxalidis reduced the competition, making additional weeding during the garlic plant cycle unnecessary for the management of this weed.

The biological control of O. latifolia by P. oxalidis was efficient without affecting the garlic plants under no-tillage.

References

• ARIANOUTSOU, M., BAZOS, I., DELIPETROU, P. and KOKKORIS, Y., 2010. The alien flora of Greece: taxonomy, life traits and habitat preferences. Biological Invasions, vol. 12, no. 10, pp. 3525-3549. http://dx.doi.org/10.1007/s10530-010-9749-0
  » http://dx.doi.org/10.1007/s10530-010-9749-0
• BURGER, W.C., 1991. Flora Costaricensis Chicago: Field Museum of Natural History. Oxalidaceae, Fieldiana, Botany, vol. 28, pp. 2-16.
• EVERARD, M., GUPTA, N., CHAPAGAIN, P.S., SHRESTHA, B.B., PRESTON, G. and TIWARI, P., 2018. Can control of invasive vegetation improve water and rural livelihood security in Nepal? Ecosystem Services, vol. 32, no. 10, pp. 125-133. http://dx.doi.org/10.1016/j.ecoser.2018.07.004
  » http://dx.doi.org/10.1016/j.ecoser.2018.07.004
• FARR, D.F. and ROSSMAN, A.Y., 2018 [viewed 27 October 2020]. Fungal Databases [online]. Available from: https://nt.ars-grin.gov/fungaldatabases/
  » https://nt.ars-grin.gov/fungaldatabases/
• GUERRA, F.A., DE ROSSI, R.L., BRÜCHER, E., VULETIC, E., PLAZAS, M.C., GUERRA, G.D. and DUCASSE, D.A., 2019. Occurrence of the complete cycle of Puccinia sorghi Schw. in Argentina and implications on the common corn rust epidemiology. European Journal of Plant Pathology, vol. 154, no. 2, pp. 171-177. http://dx.doi.org/10.1007/s10658-018-01645-3
  » http://dx.doi.org/10.1007/s10658-018-01645-3
• IRELAND, K.B., HUNTER, G.C., WOOD, A., DELAISSE, C. and MORIN, L., 2019. Evaluation of the rust fungus Puccinia rapipes for biological control of Lycium ferocissimum (African boxthorn) in Australia: life cycle, taxonomy and pathogenicity. Fungal Biology, vol. 123, no. 11, pp. 811-823. http://dx.doi.org/10.1016/j.funbio.2019.08.007 PMid:31627857.
  » http://dx.doi.org/10.1016/j.funbio.2019.08.007
• KIRK, P.M., CANNON, P.F., MINTER, D.W. and STALPERS, J., 2008. Dictionary of the fungi 10th ed. Wallingford: CABI. 771 p.
• KÖPPEN, W., 1936. Das geographische system der klimate. In: W. KÖPPEN and R. GEIGER, eds. Handbuch der Klimatologie Berlin: Gebrüder Bornträger, pp. 1-44.
• LEE, S.H., LEE, C.K., CHO, S.E. and SHIN, H.D., 2019. First report of rust caused by Puccinia oxalidis on Oxalis debilis var. corymbosa in Korea. Plant Disease, vol. 103, no. 1, pp. 148-149. http://dx.doi.org/10.1094/PDIS-05-18-0777-PDN
  » http://dx.doi.org/10.1094/PDIS-05-18-0777-PDN
• MAHARJAN, S., DEVKOTA, A., SHRESTHA, B.B., BANIYA, C.B., RANGASWAMY, M. and JHA, P.K., 2020. Prevalence of Puccinia abrupta var. partheniicola and its impact on Parthenium hysterophorus in Kathmandu Valley, Nepal. Journal of Ecology and Environment, vol. 44, no. 1, pp. 1-7. http://dx.doi.org/10.1186/s41610-020-00168-5
  » http://dx.doi.org/10.1186/s41610-020-00168-5
• MARIN-FELIX, Y., GROENEWALD, J.Z., CAI, L., CHEN, Q., MARINCOWITZ, S., BARNES, I., BENSCH, K., BRAUN, U., CAMPORESI, E., DAMM, U., DE BEER, Z.W., DISSANAYAKE, A., EDWARDS, J., GIRALDO, A., HERNÁNDEZ-RESTREPO, M., HYDE, K.D., JAYAWARDENA, R.S., LOMBARD, L., LUANGSA-ARD, J., MCTAGGART, A.R., ROSSMAN, A.Y., SANDOVAL-DENIS, M., SHEN, M., SHIVAS, R.G., TAN, Y.P., VAN DER LINDE, E.J., WINGFIELD, M.J., WOOD, A.R., ZHANG, J.Q., ZHANG, Y. and CROUS, P.W., 2017. Genera of phytopathogenic fungi: Gophy 1. Studies in Mycology, vol. 86, pp. 99-216. http://dx.doi.org/10.1016/j.simyco.2017.04.002 PMid:28663602.
  » http://dx.doi.org/10.1016/j.simyco.2017.04.002
• ROYO-ESNAL, A. and LÓPEZ FERNÁNDEZ, M.L., 2010. Modelling leaf development in Oxalis latifolia. Spanish Journal of Agricultural Research, vol. 8, no. 2, pp. 419-424. http://dx.doi.org/10.5424/sjar/2010082-1214
  » http://dx.doi.org/10.5424/sjar/2010082-1214
• ŠAFRÁNKOVÁ, I., 2014. Occurrence of rust disease caused by Puccinia oxalidis on Oxalis triangularis in the Czech Republic-Short cCommunication. Plant Protection Science, vol. 50, no. 1, pp. 17-18. http://dx.doi.org/10.17221/19/2013-PPS
  » http://dx.doi.org/10.17221/19/2013-PPS
• SHRESTHA, B.B., SHRESTHA, U.B., SHARMA, K.P., THAPA-PARAJULI, R.B., DEVKOTA, A. and SIWAKOTI, M., 2019. Community perception and prioritization of invasive alien plants in Chitwan-Annapurna Landscape, Nepal. Journal of Environmental Management, vol. 229, no. 1, pp. 38-47. http://dx.doi.org/10.1016/j.jenvman.2018.06.034 PMid:30032998.
  » http://dx.doi.org/10.1016/j.jenvman.2018.06.034
• TALHINHAS, P., CARVALHO, R., FIGUEIRA, R. and RAMOS, A.P., 2019. An annotated checklist of rust fungi (Pucciniales) occurring in Portugal. Sydowia, vol. 71, pp. 65-84. http://dx.doi.org/10.12905/0380.sydowia71-2019-0065
  » http://dx.doi.org/10.12905/0380.sydowia71-2019-0065
• TREWAVAS, A., 2004. A critical assessment of organic farming-and-food assertions with particular respect to the UK and the potential environmental benefits of no-till agriculture. Crop Protection (Guildford, Surrey), vol. 23, no. 9, pp. 757-781. http://dx.doi.org/10.1016/j.cropro.2004.01.009
  » http://dx.doi.org/10.1016/j.cropro.2004.01.009
• UEDA, H., KUROSE, D., KUGIMIYA, S., MITSUHARA, I., YOSHIDA, S., TABATA, J., SUZUKI, K. and KITAMOTO, H..2018. Disease severity enhancement by an esterase from non-phytopathogenic yeast Pseudozyma antarctica and its potential as adjuvant for biocontrol agents. Scientific Reports, vol. 8, no. 1, pp. 16455. http://dx.doi.org/10.1038/s41598-018-34705-z PMid:30405193.
  » http://dx.doi.org/10.1038/s41598-018-34705-z
• VACACELA AJILA, H.E., FERREIRA, J.A.M., COLARES, F., OLIVEIRA, C.M., BERNARDO, A.M.G., VENZON, M. and PALLINI, A., 2018. Ricoseius loxocheles (Acari: Phytoseiidae) is not a predator of false spider mite on coffee crops: What does it eat? Experimental & Applied Acarology, vol. 74, no. 1, pp. 1-11. http://dx.doi.org/10.1007/s10493-018-0211-9 PMid:29383531.
  » http://dx.doi.org/10.1007/s10493-018-0211-9
• VAN DER MERWE, M., ERICSON, L., WALKER, J., THRALL, P.H. and BURDON, J.J., 2007. Evolutionary relationships among species of Puccinia and Uromyces (Pucciniaceae, Uredinales) inferred from partial protein coding gene phylogenies. Mycological Research, vol. 111, no. Pt 2, pp. 163-175. http://dx.doi.org/10.1016/j.mycres.2006.09.015 PMid:17324755.
  » http://dx.doi.org/10.1016/j.mycres.2006.09.015
• VERSLUYS, W.S., 1977. New plant disease record in New Zealand: Puccinia oxalidis on Oxalis. New Zealand Journal of Agricultural Research, vol. 20, no. 3, pp. 429-430. http://dx.doi.org/10.1080/00288233.1977.10427355
  » http://dx.doi.org/10.1080/00288233.1977.10427355
• WANG, E., DONG, C., PARK, R.F. and ROBERTS, T.H., 2019. Carotenoid complement of rust spores: variation among species and pathotype. Phytochemistry, vol. 161, no. 5, pp. 139-148. http://dx.doi.org/10.1016/j.phytochem.2019.02.007 PMid:30836233.
  » http://dx.doi.org/10.1016/j.phytochem.2019.02.007

Publication Dates

• Publication in this collection
  15 Dec 2021
• Date of issue
  2024

History

• Received
  24 Feb 2021
• Accepted
  06 Sept 2021