11 Endophytes as Plant Nutrient Uptake-Promoter in Plants
249
design of agricultural systems that aims to reduce inputs of chemicals and using the
endophyte microbes to maximize the efficiency of such resources might be of great
importance (Maheshwari 2017; Tilman et al. 2002). Thus, the endophytic fungi that
enhance the nutrient uptake by their plant hosts (Lledó et al. 2015) could play an
important role in more sustainable agriculture systems. This may allow reducing the
number of chemical fertilizers for enhancing plant growth, and consequently productivity (Silveira and Kohmann 2020), or by improving food or feed nutritional quality
by increasing the concentration of some minerals in the edible parts, especially when
considering the requirement of some essential minerals for animals and humans, such
as I, Fe, Zn, and Se, that usually present deficiency (Graham et al. 2007; White and
Broadley 2005).
As supporting knowledge for the eventual use of endophytes with that purpose,
several studies have reported the enhancement of the nutrient uptake in plants caused
by endophytes, as summarized in Table 11.1. The endophyte Epichloë festucae
Leuchtm., Schardl and Siegel has been found to increase the uptake of P, N, Zn, Ca, or
Mg by Festuca rubra L. plants (Vázquez de Aldana et al. 2013; Zabalgogeazcoa et al.
2006) and accumulation of Mn by Lolium perenne L. in its herbage (Soto-Barajas
et al. 2016). Other endophytes belonging to Neotyphodium genus have been reported
in increasing the concentration of Zn and Mo in L. perenne (Malinowski et al. 2004)
and the concentration of P, Ca, or Zn in Festuca arundinacea Schreb. (Malinowski
et al. 2000). According to Lledó et al. (2015), when the endophyte Stemphylium
globuliferum (Vestergr.) Simmons was inoculated in Poa pratensis L., its herbage
showed higher values in the concentration of Ca (from 0.78 to 0.90 mg/kg), Mg (from
0.31 to 0.36 mg/kg), and Sr (from 68.07 to 77.68 mg/kg) in comparison to that of
uninoculated plants. Authors reported a significant increase in the Al, B, Fe, Li, Mo,
Ni, and Ti uptake when plants were inoculated with Epicoccum nigrum Link, while
the inoculation of Fusarium lateritium Nees in P. pratensis caused an increase in
the concentration of Fe, Ni, and Zn in the herbage by 31%, 32%, and 16%, respectively, in comparison with the uninoculated controls. An increase in the Fe uptake
by endophyte-infected plants has also been reported by Bartholdy et al. (2001), and
Johnson et al. (2013), when studied the influence of Phialocephala fortinii Wang
and Wilcox, and Epichloë/Neotyphodium on forest tree species and Lolium perenne,
respectively. Also, Phomopsis liquidambari Chang, Jiang, and Chi, a mutualistic rice
symbiont, promoted rice growth and grain yield at the same time that significantly
reduced the amount of soil N fertilizer required for optimum plant growth (Li et al.
2009; Yuan et al. 2007).
Although most of the studies have been focused on grass species hosts, the positive influence of endophytes on the uptake and later accumulation of minerals has
also been reported in other host families, such as legumes. Thus, in Ornithopus
compressus L. plants, the endophytes Stemphylium sp., Fusarium sp., Sordaria fimicola (Roberge ex Desm.) Ces. and De Not., and Sporormiella intermedia (Auersw.)
Ahmed and Cain ex Kobayasi were found to cause a higher accumulation of B, Mo, P,
S and Zn in the herbage than in controls (endophyte-free plants) in a study conducted
by Santamaria et al. (2017). Likewise, Stemphylium globuliferum caused a higher
accumulation of Ca, Cd, Cu, Mn, Pb and Zn (more than 31, 217, 66, 14, 305 and
249
design of agricultural systems that aims to reduce inputs of chemicals and using the
endophyte microbes to maximize the efficiency of such resources might be of great
importance (Maheshwari 2017; Tilman et al. 2002). Thus, the endophytic fungi that
enhance the nutrient uptake by their plant hosts (Lledó et al. 2015) could play an
important role in more sustainable agriculture systems. This may allow reducing the
number of chemical fertilizers for enhancing plant growth, and consequently productivity (Silveira and Kohmann 2020), or by improving food or feed nutritional quality
by increasing the concentration of some minerals in the edible parts, especially when
considering the requirement of some essential minerals for animals and humans, such
as I, Fe, Zn, and Se, that usually present deficiency (Graham et al. 2007; White and
Broadley 2005).
As supporting knowledge for the eventual use of endophytes with that purpose,
several studies have reported the enhancement of the nutrient uptake in plants caused
by endophytes, as summarized in Table 11.1. The endophyte Epichloë festucae
Leuchtm., Schardl and Siegel has been found to increase the uptake of P, N, Zn, Ca, or
Mg by Festuca rubra L. plants (Vázquez de Aldana et al. 2013; Zabalgogeazcoa et al.
2006) and accumulation of Mn by Lolium perenne L. in its herbage (Soto-Barajas
et al. 2016). Other endophytes belonging to Neotyphodium genus have been reported
in increasing the concentration of Zn and Mo in L. perenne (Malinowski et al. 2004)
and the concentration of P, Ca, or Zn in Festuca arundinacea Schreb. (Malinowski
et al. 2000). According to Lledó et al. (2015), when the endophyte Stemphylium
globuliferum (Vestergr.) Simmons was inoculated in Poa pratensis L., its herbage
showed higher values in the concentration of Ca (from 0.78 to 0.90 mg/kg), Mg (from
0.31 to 0.36 mg/kg), and Sr (from 68.07 to 77.68 mg/kg) in comparison to that of
uninoculated plants. Authors reported a significant increase in the Al, B, Fe, Li, Mo,
Ni, and Ti uptake when plants were inoculated with Epicoccum nigrum Link, while
the inoculation of Fusarium lateritium Nees in P. pratensis caused an increase in
the concentration of Fe, Ni, and Zn in the herbage by 31%, 32%, and 16%, respectively, in comparison with the uninoculated controls. An increase in the Fe uptake
by endophyte-infected plants has also been reported by Bartholdy et al. (2001), and
Johnson et al. (2013), when studied the influence of Phialocephala fortinii Wang
and Wilcox, and Epichloë/Neotyphodium on forest tree species and Lolium perenne,
respectively. Also, Phomopsis liquidambari Chang, Jiang, and Chi, a mutualistic rice
symbiont, promoted rice growth and grain yield at the same time that significantly
reduced the amount of soil N fertilizer required for optimum plant growth (Li et al.
2009; Yuan et al. 2007).
Although most of the studies have been focused on grass species hosts, the positive influence of endophytes on the uptake and later accumulation of minerals has
also been reported in other host families, such as legumes. Thus, in Ornithopus
compressus L. plants, the endophytes Stemphylium sp., Fusarium sp., Sordaria fimicola (Roberge ex Desm.) Ces. and De Not., and Sporormiella intermedia (Auersw.)
Ahmed and Cain ex Kobayasi were found to cause a higher accumulation of B, Mo, P,
S and Zn in the herbage than in controls (endophyte-free plants) in a study conducted
by Santamaria et al. (2017). Likewise, Stemphylium globuliferum caused a higher
accumulation of Ca, Cd, Cu, Mn, Pb and Zn (more than 31, 217, 66, 14, 305 and