Heating quinoa shoots results in yield loss by inhibiting fruit production and delaying maturity

Abstract

Increasing global temperatures and a growing world population create the need to develop crop varieties that provide higher yields in warmer climates. There is growing interest in expanding quinoa cultivation, because of the ability of quinoa to produce nutritious grain in poor soils, with little water and at high salinity. The main limitation to expanding quinoa cultivation, however, is the susceptibility of quinoa to temperatures above approximately 32°C. This study investigates the phenotypes, genes and mechanisms that may affect quinoa seed yield at high temperatures. Using a differential heating system where only roots or only shoots were heated, quinoa yield losses were attributed to shoot heating. Plants with heated shoots lost 60-85% yield as compared with control plants. Yield losses were the result of lower fruit production, which lowered the number of seeds produced per plant. Furthermore, plants with heated shoots had delayed maturity and greater non-reproductive shoot biomass, whereas plants with both heated roots and heated shoots produced higher yields from the panicles that had escaped the heat, compared with the control. This suggests that quinoa uses a type of avoidance strategy to survive heat. Gene expression analysis identified transcription factors differentially expressed in plants with heated shoots and low yield that had been previously associated with flower development and flower opening. Interestingly, in plants with heated shoots, flowers stayed closed during the day while the control flowers were open. Although a closed flower may protect the floral structures, this could also cause yield losses by limiting pollen dispersal, which is necessary to produce fruit in the mostly female flowers of quinoa.

Keywords: RNA-seq; fruit production; heat; phenomics; plant maturity; quinoa; yield.

Figure 1

Yield analysis. (a) Yield per plant for each treatment in experimental round 1 (n = 15 plants). (b) Yield per plant for each treatment in experimental round 2 (n = 15 plants). (c) Average normalized seed area per plant for each treatment (n = 15 plants). (d) Average estimated individual seed weight per plant for each treatment (n = 15 plants). (e) Estimated number of seeds produced per plant for each treatment (n = 15 plants). Letters above boxes represent statistical significance at P < 0.05 from a Wilcoxon rank sum test.

Figure 2

Yield analysis by panicle type. (a) Locations of the main panicle (the first panicle to emerge; orange), secondary panicles at the tip of each branch (emerging after the main panicle; blue) and tertiary panicles from nodes within branches (emerging after the secondary panicles; red). (b) Yield from the main panicle of each plant for each treatment (n = 15). (c) Number of seeds produced per main panicle for each treatment (n = 15). (d) Average seed weight per main panicle for each treatment (n = 15). (e) Average main panicle normalized seed area per plant for each treatment (n = 15). (f) Aggregated yield from all secondary panicles in each plant, for each treatment (n = 15). (g) Number of secondary panicles produced by each plant for each treatment (n = 15). (h) Total tertiary panicle yield per plant for each treatment (n = 15). (i) Number of seeds produced from all tertiary panicles in each plant for each treatment (n = 15). (j) Average tertiary panicle seed weight per plant for each treatment (n = 15). (k) Average normalized tertiary panicle seed area from each plant and for each treatment (n = 15). (l) Number of tertiary panicles produced by each plant for each treatment (n = 15). Control, roots and shoots held at 22°C; HR, heated roots, with roots held at 30°C and shoots held at 22°C; HS, heated shoots, with shoots held at 35°C and roots held at 22°C; HRS, heated roots and shoots, with roots at held at 30°C and shoots held at 35°C. Letters above boxes represent statistical significance at P < 0.05 from a Wilcoxon rank sum test.

Figure 3

Analysis of the yield of secondary panicles. (a) Yield of individual secondary panicles by position in the plant for each treatment (n = 1–7 secondary panicles, depending on position). (b) Yield from individual secondary panicles heat treated for 0, 1, 2, 4, 6, 8 or 11 days: n = 9 (control), 22 (HR), 86 (HRS) and 72 (HS) panicles for 0 days; n = 46 (control), 21 (HR), 6 (HRS) and 4 (HS) panicles for 1 day; n = 8 (HRS) panicles for 2 days; n = 19 (control), 34 (HR), 5 (HRS) and 3 (HS) panicles for 4 days; n = 59 (control), 36 (HR), 1 (HRS) and 6 (HS) panicles for 6 days; n = 9 (control), 11 (HR) and 6 (HS) panicles for 8 days; n = 10 (control), 48 (HR), 79 (HRS) and 101 (HS) panicles for 11 days. Control, roots and shoots held at 22°C; HR, heated roots, with roots held at 30°C and shoots held at 22°C; HS, heated shoots, with shoots held at 35°C and roots held at 22°C; HRS, heated roots and shoots, with roots at held at 30°C and shoots held at 35°C. Error bars represent standard deviation.

Figure 4

Main panicle flower analysis. (a) Fruit production measured on days 2, 24 and 45 after heat treatment ended. (b) Flower density in the most apical 5 cm of the main panicle measured on days 2, 24 and 45 after heat treatment ended. Curves resulting from a LOESS (locally estimated scatter‐plot smoothing) polynomial regression are shown (n = 30 main panicles, for each time point and each treatment). Letters next to curves represent statistical significance at P < 0.05 from a Kolmogorov–Smirnov test. (c) Flowers from the main panicle for each treatment imaged after 9 days of heat treatment, 18 days after heat treatment ended and 40 days after heat treatment ended. All images have been scaled to the same scale bar.

Figure 5

Analysis of main panicle structure. (a) Area of each main panicle at harvest per treatment (n = 15). (b) Weight of each main panicle at harvest for each treatment (n = 15). (c) Main panicle solidity for each plant and for each treatment (n = 15). (d) Segment of a quinoa main panicle showing fruit (red arrows) and unfertilized flowers (yellow arrows). (e) Number of branches in each main panicle for each treatment (n = 15). (f) Example images of the main panicle from each treatment group (representative median image for area) at harvest. Control, roots and shoots held at 22°C; HR, heated roots, with roots held at 30°C and shoots held at 22°C; HS, heated shoots, with shoots held at 35°C and roots held at 22°C; HRS, heated roots and shoots, with roots at held at 30°C and shoots held at 35°C. Letters above boxes represent statistical significance at P < 0.05 from a Wilcoxon rank sum test.

Figure 6

Shoot size and maturity. (a) Shoot dry weight (g) with 1 day of heat, 11 days of heat and at harvest (n = 9 for each treatment for days 1 and 11 of heat treatment, and n = 15 for each treatment at harvest). (b) Shoot dry weight without panicles at harvest (n = 15 for each treatment). (c) Normalized area for each plant and for each treatment (n = 15). (d) Solidity for each plant and for each treatment (n = 15). (e) Percentage yellow area for each treatment per plant (n = 15). (f) Example images from each treatment group (representative median image) classified into yellow or green pixels by naive Bayes classifier from plantcv. Control, roots and shoots held at 22°C; HR, heated roots, with roots held at 30°C and shoots held at 22°C; HS, heated shoots, with shoots held at 35°C and roots held at 22°C; HRS, heated roots and shoots, with roots at held at 30°C and shoots held at 35°C. Letters above boxes represent statistical significance at P < 0.05 from a Wilcoxon rank sum test.

Figure 7

Differentially expressed genes by treatment and day of sampling. (a) Venn diagram of differentially expressed genes from control on day 1 of heat treatment and day 11 of heat treatment (n = 3 for each time point and each treatment). Overlapping genes in treatments with reduced yield are shown in bold. (b) Differentially expressed genes overlapping between day 1 and day 11 in treatments with reduced yield (HRS and HS).

Figure 8

Shoot heating affected floral opening compared with the control. (a) Representative images of open and closed quinoa flowers. (b) Percentage of open hermaphrodite flowers in the main panicle on day 6 of heat treatment (n = 15). Control, roots and shoots held at 22°C; HR, heated roots, with roots held at 30°C and shoots held at 22°C; HS, heated shoots, with shoots held at 35°C and roots held at 22°C; HRS, heated roots and shoots, with roots at held at 30°C and shoots held at 35°C. Letters above boxes represent statistical significance at P < 0.05 from a Wilcoxon rank sum test. (c) Representative images of control and heated shoot main panicles.