Heterosis for Interactions between Insect Herbivores and 3-Line Hybrid Rice under Low and High Soil Nitrogen Conditions

Abstract

Hybrid rice results from crossing a male-sterile line (the A line) with a pollen doner (the restorer or R line). In 3-line hybrid breeding systems, a fertile B line is also required to maintain A line populations. Heterosis is defined as a condition of traits whereby the hybrid exceeds the average of the parental lines. Heterobeltiosis is where the hybrid exceeds both parents. Hybrid rice may display heterosis/heterobeltiosis for growth, yield and resistance to herbivores, among other traits. In a greenhouse experiment, we assessed the frequency of heterosis for resistance to the brown planthopper (Nilaparvata lugans (BPH)), whitebacked planthopper (Sogatella furcifera (WBPH)) and yellow stemborer (Scirpophaga incertulas (YSB)) in eight hybrids under varying soil nitrogen conditions. We also assessed plant biomass losses due to herbivore feeding as an approximation of tolerance (the plant's capacity to compensate for damage). Nitrogen reduced resistance to all three herbivores but was also associated with tolerance to WBPH and YSB based on improved plant survival, growth and/or yields. Plant biomass losses per unit weight of WBPH also declined under high nitrogen conditions for a number of hybrids, and there were several cases of overcompensation in rice for attacks by this herbivore. There was one case of nitrogen-related tolerance to BPH (increased grain yield) for a hybrid line with relatively high resistance, likely due to quantitative traits. Heterosis and heterobeltiosis were not essential to produce relatively high herbivore resistance or tolerance across hybrids.

Keywords: brown planthopper; fertilizer; herbivory tolerance; heterobeltiosis; heterosis; host plant resistance; plant physiology; rice herbivores; whitebacked planthopper; yellow stemborer.

Figure 1

Biomass of brown planthopper (brown circles), whitebacked planthopper (blue triangles), and yellow stemborer (green squares) on eight hybrid lines and their associated parental lines under low (light colored symbol) and high (dark colored symbols) nitrogen conditions. The results for the (A) IR82396H, (B) IR82391H, (C) IR84714H, (D) IR85471H, (E) IR81954H, (F) IR80637H, (G) IR82385H and (H) IR82363H hybrids and their parental lines are shown. Means and standard errors are indicated (N = 6). The results of univariate GLMs are indicated for main factors (I = insect species, F = fertilizer level, P = plant type) and their significant two-way interactions are indicated together with significance levels denoted as ** = p ≤ 0.01 and *** = p ≤ 0.005. The full results of GLMs are presented in Table S4. Separate results for each insect species are presented in Section 3.3.

Figure 2

(A–H) Total dry weight (biomass) of brown planthopper and (I–P) plant biomass loss per unit planthopper weight on eight hybrids (H on x-axes) and their associated parental lines (A line, B line and R line, A, B and R on the x-axes, respectively) in a greenhouse experiment. The results are presented for the (A,I) IR82396H group, (B,J) IR82391H group, (C,K) IR84714H group, (D,L) IR85471H group, (E,M) IR81954H group, (F,N) IR80637H group, (G,O) IR82385H group and (H,P) IR82363H group. The results of univariate GLMs are indicated with each graph as A = accession, N = nitrogen and A × N = accession × nitrogen interaction with * = p ≤ 0.05, ** = p ≤ 0.01 and *** = p ≤ 0.005. Lowercase letters indicate homogenous plant types (Tukey p > 0.05). Means and standard errors (N = 6) are shown. Average parameter values for A lines (dashed lines) and B lines (solid lines) are indicated for plants grown under low (black) and high (blue) nitrogen conditions. Cases of heterosis are indicated in Table 1. See Tables S5 and S6 for details of other BPH fitness parameters and plant responses.

Figure 3

(A–H) Total dry weight (biomass) of whitebacked planthopper and (I–P) plant biomass loss per unit planthopper weight on eight hybrids (H on x-axes) and their associated parental lines (A line, B line and R line, A, B and R on the x-axes, respectively) in a greenhouse experiment. The results are presented for the (A,I) IR82396H group, (B,J) IR82391H group, (C,K) IR84714H group, (D,L) IR85471H group, (E,M) IR81954H group, (F,N) IR80637H group, (G,O) IR82385H group and (H,P) IR82363H group. The results of univariate GLMs are indicated with each graph as A = accession, N = nitrogen and A × N = accession × nitrogen interaction with * = p ≤ 0.05, ** = p ≤ 0.01 and *** = p ≤ 0.005. Lowercase letters indicate homogenous plant types (Tukey p > 0.05). Means and standard errors (N = 6) are shown. Average parameter values of A lines (dashed lines) and B lines (solid lines) are indicated for plants grown under low (black) and high (blue) nitrogen conditions. Cases of heterosis are indicated in Table 2. See Tables S9 and S10 for details of other WBPH fitness parameters and plant responses.

Figure 4

(A–H) Total dry weight (biomass) of yellow stemborer and (I–P) plant biomass loss per unit planthopper weight on eight hybrids (H on the x-axes) and their associated parental lines (A line, B line and R line, A, B and R on the x-axes, respectively) in a greenhouse experiment. The results are presented for the (A,I) IR82396H group, (B,J) IR82391H group, (C,K) IR84714H group, (D,L) IR85471H group, (E,M) IR81954H group, (F,N) IR80637H group, (G,O) IR82385H group and (H,P) IR82363H group. The results of univariate GLMs are indicated with each graph as A = accession, N = nitrogen and A × N = accession × nitrogen interaction with * = p ≤ 0.05, ** = p ≤ 0.01 and *** = p ≤ 0.005. Lowercase letters indicate homogenous plant types (Tukey p > 0.05). Means and standard errors (N = 2–6, see Table S13) are shown. Average parameter values of A lines (dashed lines) and B lines (solid lines) are indicated for plants grown under low (black) and high (blue) nitrogen conditions. Cases of heterosis are indicated in Table 3. See Tables S13 and S14 for details of other WBPH fitness parameters and plant responses.