The roles of jasmonate (JA) signaling in nitrogen uptake and allocation in rice (Oryza sativa L.)

Authors: WU, XIAOYING - Huzhou University; LIN, XIANHUI - Fujian Agriculture And Forest University; Baerson, Scott; DING, CHAOHUI - Fujian Agriculture And Forest University; ZHANG, LIQIN - Huzhou University; WU, CCHOUFEI - Huzhou University; SONG, YUANYUAN - Fujian Agriculture And Forest University; ZENG, RENSEN - Fujian Agriculture And Forest University

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/18/2018
Publication Date: 9/24/2018
Citation: Wu, X., Lin, X., Baerson, S.R., Ding, C., Zhang, L., Wu, C., Song, Y., Zeng, R. 2018. The roles of jasmonate (JA) signaling in nitrogen uptake and allocation in rice (Oryza sativa L.). New Phytologist. https://doi.org/10.1111/pce.13451.
DOI: https://doi.org/10.1111/pce.13451

Interpretive Summary: The plant hormone jasmonic acid is well known to play a central role in mediating the defensive responses mounted by plants in response to insect herbivore infestations. These defensive responses fall into two general categories. Those which involve the production of defensive compounds such as allelochemicals, which impede the growth and/or development of herbivores, are referred to as resistance responses. The second major category, referred to as tolerance responses, involves the mobilization of nutrients away from plant parts subjected to herbivore feeding, and sequestering these nutrients for later use during plant recovery from insect damage. Since plants often employ both strategies, competition can occur between these two response types, as resistance requires the synthesis of large quantities of various allelochemicals and is therefore highly resource-intensive, whereas tolerance results in a localized depletion of nutrient resources. While the molecular details surrounding the involvement of jasmonic acid in insect resistance have been extensively studied, far less is known concerning the role played by this hormone in insect tolerance. In our study we show that jasmonic acid also effects a large number of proteins involved in the utilization of the critical mineral nutrient nitrogen (N), leading to changes in the uptake of N from the environment, its movement within plants, and its availability for various biochemical processes. The evidence we have obtained also indicates that a significant amount of N mobilized from jasmonic acid-treated leaves is derived from the disassembly of leaf chloroplasts and the breakdown of chloroplast constituent proteins. Taken together, our results indicate that jasmonic acid plays a major role in insect tolerance responses, and coordinates the re-allocation and uptake of N resources in rice plants in response to insect herbivore infestations.

Technical Abstract: Herbivore damage by chewing insects activates jasmonate (JA) signaling. It is well-known that the JA signaling can elicit systemic defense responses and increased production of defensive compounds in plants. Few details are known, however, concerning the mechanism whereby JA signaling modulates nutrient uptake and allocation in plants in response to herbivory. The present work demonstrates that exogenous applications of methyl jasmonate (MeJA) to rice seedlings leads to significantly reduced nitrogen (N) uptake levels in roots, concomitant with an enhancement of nitrogen allocation to these tissues. JA negatively affected N uptake in roots, and reduced the translocation of recently-absorbed 15N from roots to leaves, likely occurring as a result of down-regulation of NiR, GS1;2, and multiple nitrate and ammonium transporters. Additionally, proteomic and RT-qPCR experiments provided evidence suggesting that plastid disassembly contributes to the release of N in leaves. MeJA treatment also significantly increased the expression of glutamate dehydrogenase genes GDH1 and GDH2 in leaves. Collectively, these results indicate that JA signaling mediates large-scale systemic changes to N allocation and uptake in rice plants in response to insect herbivory.