Heterodera schachtii infection affects nitrogen metabolism in Arabidopsis thaliana

Abstract

Nitrogen metabolism is important for physiological processes during normal growth and development, as well as plant defence responses. Second‐stage juveniles of the cyst nematode Heterodera schachtii penetrate into the root and initiate permanent feeding sites called syncytia, from which they draw all necessary nutrients. To unravel whether the cyst nematode infestation changes nitrogen metabolism, the enzymatic activity and gene expression of nitrate (NIA) and nitrite (NIR) reductases and glutamate dehydrogenase (GDH), as well as levels of the metabolites nitrates, nitrites, and ammonium ions were estimated both locally in inoculated roots and systemically in shoots of inoculated Arabidopsis thaliana plants at 3, 7, and 15 days post‐inoculation (dpi). Moreover, gene expression of long hypocotyle 5 (HY5), a basic‐region leucine zipper (bZIP) transcription factor, was also determined, to learn more about the potential transcriptional regulation of the analysed enzymes. It was shown that the activity of nitrogen‐related enzymes and the content of metabolites fluctuated during the whole period of infection. These results were accompanied by organ‐specific and dpi‐dependent gene expression patterns. The high gene expression level of HY5 in infected roots at 7 and 15 dpi coexisted with enhanced expression of NIA1 and NIR1 at 7 dpi and NIA2 at 15 dpi. Enhanced HY5 expression level in shoots of infected plants at 15 dpi was followed by up‐regulation of NIA1 expression, suggesting that HY5 may regulate the gene expression of NIA and NIR during nematode infection. Our results indicate that changes in plant nitrogen metabolism occur during cyst nematode infection.

Cyst Nematode Infection Elicits Alteration in the Level of Reactive Nitrogen Species, Protein S-Nitrosylation and Nitration, and Nitrosoglutathione Reductase in Arabidopsis thaliana Roots

“…It was shown that MPKs, including soybean homologs of A. thaliana MPK3 and MPK6 described above, had a defensive role during the G. max response to H. glycines infection. Interestingly, in addition to the argumentation presented above, another face of the NO-MPKs interaction should be considered, especially taking into account the results presented earlier by our team in the article on the metabolism of nitrogen in H. schachtii-infected A. thaliana plants [23]. Siddique et al [20] showed elevated H 2 O 2 production in A. thaliana roots as a result of the H. schachtii infestation.…”

“…Melillo et al [21] found a swift NO presence at 12 h after M. incognita infection in tomato roots, whereas Zhou et al [22] pointed to enhanced transcript levels of NO biosynthetic (nitrate reductase) and signaling (S-nitrosoglutathione reductase) genes at 7 days after infection. Therefore, on the basis of the above described data and our recently published results presenting significant alterations in the activity of nitrate and nitrite reductases and nitrate/nitrite amounts in A. thaliana plants infected with H. schachtii [23], it would be supposed that the changes in nitrogen metabolism induced by cyst nematode infection may coexist with altered RNS metabolism in infected plants. Thus, the aim of this research was to study the effect of H. schachtii infection on RNS metabolism in A. thaliana roots.…”

“…Furthermore, Wang et al [34] proved that H 2 O 2 -mediated activation of MPK6 in roots of A. thaliana led to the phosphorylation of nitrate reductase 2 (NIA2) by MPK6, resulting in increased nitrate reductase enzyme activity and NO liberation. It cannot be overlooked that enhanced transcript level of the NIA2 gene was responsible for the increased enzyme activity of nitrate reductase in H. schachtii-infected A. thaliana roots at 3 dpi [23]. These data indicate that, at least to some extent observed by us herein, the intense NO burst in the cyst nematode infested A. thaliana roots at the early stage of infection resulted from higher (3-fold) nitrate reductase activity in infected roots than in control samples ( Figure 10) [23].…”

“…It cannot be overlooked that enhanced transcript level of the NIA2 gene was responsible for the increased enzyme activity of nitrate reductase in H. schachtii-infected A. thaliana roots at 3 dpi [23]. These data indicate that, at least to some extent observed by us herein, the intense NO burst in the cyst nematode infested A. thaliana roots at the early stage of infection resulted from higher (3-fold) nitrate reductase activity in infected roots than in control samples ( Figure 10) [23]. Non-enzymatic production of NO from nitrites in the presence of reduced ascorbate [7] cannot be excluded because of a decrease in nitrite content at 3 dpi [23] and an increase in reduced ascorbate content in H. schachtii-infected A. thaliana roots observed [35].…”

Efficient antioxidant defence systems of spring barley in response to stress induced jointly by the cyst nematode parasitism and cadmium exposure

“…Our previous results showed that changes in plant nitrogen metabolism took place during cyst nematode infection (Labudda et al 2020a). Arginase (ARG), nitrogen metabolism-linked enzyme, was another enzyme that was analysed in these studies.…”