Cryptic CAM photosynthesis in Joshua tree (Yucca brevifolia, Y. jaegeriana)

Abstract

Joshua trees are long-lived perennial monocots native to the Mojave Desert in North America. Composed of two species, Yucca brevifolia and Y. jaegeriana (Asparagaceae), Joshua trees are imperiled by climate change, with decreases in suitable habitat predicted under future climate change scenarios. Relatively little is understood about the ecophysiology of Joshua trees across their range, including the extent to which populations are locally adapted or phenotypically plastic to environmental stress. Plants in our common gardens showed evidence of Crassulacean acid metabolism photosynthesis (CAM) in a pilot experiment, despite no prior report of this photosynthetic pathway in these species. We further studied the variation and strength of CAM within a single common garden, measuring seedlings representing populations across the range of the two species. A combination of physiology and transcriptomic data showed low levels of CAM that varied across populations but were unrelated to home environmental conditions. Gene expression confirmed CAM activity and further suggested differences in carbon and nitrogen metabolism between Y. brevifolia and Y. jaegeriana. Together the results suggest greater physiological diversity between these species than initially expected, particularly at the seedling stage, with implications for future survival of Joshua trees under a warming climate.

Keywords: CAM; Joshua tree; Mojave; Yucca; ecophysiology; photosynthesis.

Fig. 1

Variation in home climate and results from a preliminary screen of source populations of Joshua trees. (a) First two principal component axes of climate variation for natural Joshua tree populations, showing frequency of Joshua tree occurrences across climate PCA space. Background frequency plot based on occurrence data in Esque et al. (2023). PC coordinates of source populations are labeled, with shape indicative of species (square: western Joshua tree (Yucca brevifolia), circle: eastern (Yucca jaegeriana), triangle: hybrid). Garden locations in climate space are indicated by red stars. (b) Daytime expression of phosphoenolpyruvate carboxylase (PPC) copies 1 and 2 from individuals from four source populations (CS, LAR, LMV, and LWP) sampled in two common gardens (Nevada, UT). The expression shown is based on mapping to the Y. jaegeriana reference transcripts and is shown for the PPC1 and PPC2 genes that were differentially expressed between gardens. In post hoc t‐tests between gardens within each source population, only PPC2 showed differential expression, and only in LWP individuals; all other source population were not significantly different in expression between gardens (n.s.).

Fig. 2

Carbon assimilation and leaf acid accumulation in common garden‐grown Joshua trees. Mean and SE of daytime assimilation of CO₂ (a), mean nighttime assimilation (b), and mean accumulation of leaf acid (delta H⁺) (c). Means are shown across source populations, arranged first by species classification, then from west to east along the x‐axis. Shapes correspond to classification as western Joshua trees (Yucca brevifolia), eastern Joshua trees (Yucca jaegeriana), or a hybrid between the two. (d–f) points on the map showing the location of each source population, shaded by mean population value for daytime photosynthesis (d), nighttime photosynthesis (e), and acid accumulation (f).

Fig. 3

Measures of water content, water use, and maternal adult plant leaf acidity. (a) Relative water content, (b) saturated water content, and (c) carbon isotope ratio means per population with SE for common garden plants. (d) Delta H⁺ mean and SE calculated from titrations on maternal plant leaf tissue relative to offspring H⁺ measurements from the common garden, where available. Significance values in (d) are from one‐sample t‐tests (dawn vs dusk H⁺) and are indicated with asterisks: *, P < 0.05; **, P < 0.01.

Fig. 4

Overview of the citric acid cycle in Joshua trees, showing connections between carbon and nitrogen metabolism via gene expression. Mean transcript z‐score scaled TPM expression values per source population, with outliers (> 2 SD) removed, for (a) major citric acid cycle and nitrogen assimilation genes and (b) PPDK and upstream expression of NAD‐ME. Expression is shown for both daytime and nighttime samples, indicated by open (day) and black (night) bars to the left of each heatmap. Source populations are arranged across the x‐axis with western Joshua tree (Yucca brevifolia) populations to the left (blue), eastern (Y. jaegeriana) populations to the right (yellow), and the hybrid zone in the center (green), then arranged from west to east within each species. [Correction added on 17 September 2025, after first online publication: the terms ‘eastern’ and ‘western’ in the preceding sentence have been updated.] Dashed arrow below IDH indicates the possible reverse function of IDH. Genes shown are those that had the strongest between‐species difference and are purported to be expressed in the correct cellular location, based on Arabidopsis annotation (e.g. citric acid cycle genes are expected to be expressed in the mitochondria). Asterisks indicate whether a transcript had significant differential expression between time points (left of plot) or between species (below plot). Metabolites or products are shown in purple text. Abundance of citrate is shown in the center; dawn and dusk samples are colored in different hues but were analyzed together when testing between species, as there was not a significant effect of time of sampling on concentration. 2OGDH, 2‐oxoglutarate dehydrogenase; 2‐OG, 2‐oxoglutarate; AAT, aspartate aminotransferase; ACO, aconitase 3; CS, citrate synthase; GS, glutamine synthase; GOGAT, glutamine oxoglutarate aminotransferase; IDH, isocitrate dehydrogenase; MDH, malate dehydrogenase; NAD‐ME, NAD malic enzyme; OAA, oxaloacetate; PDH, pyruvate dehydrogenase; PEP, phosphoenolpyruvate; PEPC, phosphoenolpyruvate carboxylase; PK, pyruvate kinase; PPDK, pyruvate orthophosphate dikinase; sCoA ligase, succinyl CoA ligase; SDH, succinate dehydrogenase.

Fig. 5

Gene expression of photosynthetic transcripts in Joshua tree seedlings. Mean expression and SE (in transcripts per million) per population of samples taken at night and in the morning in bacterial‐type (a) and plant‐type (b) phosphoenolpyruvate carboxylase (PPC) and PPC kinase (PPCK) (c). Shapes correspond to classification as western Joshua trees (Yucca brevifolia), eastern Joshua trees (Yucca jaegeriana), or a hybrid between the two.