The Advantages of Having Green Stems in Arid Environments

Eleinis Ávila-Lovera and Louis S. Santiago

Department of Botany and Plant Sciences, University of California, Riverside

Tasha La Doux

Figure 1. Plants with green stems are categorized by one of three types of stem photosynthesis syndromes. 1) Cactoids, like Opuntia basillaris (left) take up carbon dioxide at night; 2) Sarcocaulescent plants, e.g. Dudelya saxosa (center) recycle carbon; and 3) Retamoids, like Ephedra californica (right), have stomata in the stem epidermis allowing for gas exchange with the atmosphere.

Introduction

All plants need carbon to grow, and most plants get carbon when they take up carbon dioxide through photosynthesis with their leaves. However, in arid ecosystems, green-stemmed plants, which are able to take up carbon dioxide through photosynthesis with their stems, are common. The main limitation to photosynthesis in arid conditions is that when plants open their stomata, the tiny pores through which they absorb carbon dioxide, they also lose water (Lambers et al. 2008). Water is extremely valuable in arid ecosystems; it is the main resource that limits plant productivity on land (Chaves and Pereira 1992; Chaves et al. 2002). Reducing water loss during photosynthesis is a major advantage that green-stemmed plants have over species with normal bark (Ehleringer et al. 1987; Osmond et al. 1987; Nilsen and Sharifi 1997). Another advantage is that they can still absorb carbon dioxide for growth even when they are leafless or during dry seasons (Smith and Osmond 1987; Nilsen and Bao 1990; Tinoco-Ojanguren 2008). Such advantages might also be important during extreme drought because photosynthesis is often limited during water deficit, but can be critical for plant survival. Therefore, evaluating the costs and benefits of having green stems is important to determine how stem photosynthesis alters the balance of carbon gain and water loss during drought. Understanding these cost-benefits can also aid in predicting which species may survive future extreme droughts.

Species	Family	Common Name	Type
Ambrosia dumosa	Asteraceae	Burrow weed	Non-green
Ambrosia salsola	Asteraceae	Burrobrush, cheesebrush	Green
Bebbia juncea	Asteraceae	Sweetbush	Green
Stillingia linearifolia	Euphorbiaceae	Linear leaved stillingia	Green
Psorothamnus arborescens	Fabaceae	Mojave Indigo bush	Non-green
Senna armata	Fabaceae	Desert senna	Green
Senegalia greggi	Fabaceae	Catclaw	Non-green
Krameria bicolor	Krameriaceae	White rhatany	Green
Condea emoryi	Lamiaceae	Desert lavender	Non-green
Scutellaria mexicana	Lamiaceae	Mexican bladdersage	Green
Menodora spinescens	Oleaceae	Spiny desert olive	Green
Eriogonum inflatum	Polygonaceae	Desert trumpet	Green
Thamnosma montana	Rutaceae	Turpentine broom	Green
Simmondsia chinensis	Simmondsiaceae	Jojoba	Non-green
Larrea tridentata	Zygophyllaceae	Creosote bush	Non-green

Table 1. List of fifteen plant species studied in a desert wash (34°03’50.5’’ N, 116°03’16.3’’ W) at Joshua Tree National Park, CA, USA. Family, common name, and stem type is indicated. a Common name information taken from Calflora (www.calflora.org).

Plants with green stems are categorized by one of three types of stem photosynthesis syndromes (Figure 1). Retamoids include leafless or almost leafless woody plants that have stomata in the stem epidermis allowing for gas exchange with the atmosphere (Schaedle 1975). The other two groups of plants that photosynthesize with stems are sarcocaulescent and cactoid, with fleshy and succulent stems, respectively. These differ from the retamoids in that sarcocaulescent plants usually recycle carbon whereas cactoids take up carbon dioxide at night. Our focus in this study is on retamoid plants that have green photosynthetic stems (see species list in Table 1), and we compared them with non-green-stemmed plants. It has been noted that plants bearing green stems belong to at least 26 unrelated plant families (Nilsen 1995; Gibson 1996), which suggest that the syndrome evolved independently in different taxa, likely due as a response to life in arid environment

Mark E De Guzman

Figure 2. Left: View of the field site, a desert wash at Joshua Tree National Park near the North Entrance. Field technicians collecting data on one of the green-stemmed species, Senna armata (Fabaceae). In the background are many individuals of Larrea tridendata (Zygophyllaceae), a species with non-green stems. Right: Menodora spinescens var. mohavensis (Oleaceae) showing its green stems and some inflated fruits in October 2015.

Materials and Methods

Our study was performed in a desert wash in the Mojave Desert at Joshua Tree National Park (34° 03' 50.5" N, 116° 03' 16.3" W), near the California Riding and Hiking Trail by the north entrance of the park. The study site has a mean annual air temperature (MAT) of 18.6 °C and mean annual precipitation (MAP) of 119.1 mm. However, 2016 MAT was 19.4°C whereas precipitation was 82.3 mm. The community is dominated by creosote bush (Larrea tridendata) (Fig. 1) (Ávila-Lovera et al. 2019). We selected species with and without visually green stems (Table 1, Fig. 2). Plant water status was measured as water potential with a pressure chamber, leaf and stem gas exchange of carbon dioxide was measured using an infrared gas analyzer, and water vapor loss through the epidermis was measured using bench dehydration. These traits were measured every six weeks from spring 2016 (February) to spring 2017 (March), spanning two wet seasons and one dry season. Traits recorded for leaves and green stems included photosynthetic rate, stomatal conductance, and water-use efficiency; for the non-green stems we measured respiration rate and non-stomatal conductance. We also measured carbon and oxygen isotopic composition in photosynthetic tissues of leaves and stems at the end of both wet and dry seasons. The carbon isotopic composition of photosynthetic tissues is related to long-term water-use efficiency, with high values indicating higher long-term water-use efficiency, whereas oxygen isotopic composition is related to how dry the air was during the growing season, where higher values indicate drier air.

Figure 3. Gas-exchange data for leaves (when present) and stems of green-stemmed species, and leaves and stems of non-green-stemmed species during nine sampling campaigns from February 2016 to March 2017. (a) CO2 exchange rate, where positive values indicate net carbon uptake and negative values indicate respiration. (b) Stomatal conductance to water vapor of leaves and green stems, and non-stomatal conductance to water vapor of non-green stems. (c) Intrinsic water-use efficiency for leaves and green stems. Values shown are means of all species within each stem-type group ± standard error. Taken and modified from (Ávila-Lovera et al.)

Results and Discussion

Plants with green stems relied on their stem as the sole organ for carbon assimilation for most of the study period (Ávila-Lovera et al. 2019). All woody species with green stems had small leaves during the spring of 2016 (Fig. 2-3) and did not have any leaves all summer and fall until the following year’s winter. Plants with green stems had slightly higher water potential than plants without green stems, indicating that they maintained a better water status. However, both groups of plants experienced lower water potentials during the dry season. Green stems had higher photosynthetic rate, stomatal conductance and water loss through the epidermis than leaves of non-green-stemmed plants when normalized per area of exposed tissue, which yielded similar intrinsic water-use efficiency in both types of organs (Fig. 3). When looking at whole-plant integrated annual carbon gain, calculated from photosynthetic rate measures integrated across the year, we found no differences between green stems and leaves of non-green stemmed species.

We found partial support for higher water-use efficiency in stems than leaves based on the carbon isotopic composition data (Ávila-Lovera et al. 2019).. Furthermore, carbon isotopic composition of green stems was statistically higher than that of leaves of the same species in only one of eight green-stemmed species studied that had both leaves and green stems during the wet season of 2016. Nitrogen content in leaves and stems of green-stemmed species was also higher than in leaves and stems of non-green-stemmed species, which partially explains the higher photosynthetic performance in green stems than leaves of non-green stemmed species.

Green stems had higher water loss through the epidermis than leaves and stems of non-green-stemmed plants (Ávila-Lovera et al. 2019). This result raises questions about the possible trade-off between carbon gain and water loss through the epidermis in green stems and how this may affect plant responses to current and future droughts (Ávila-Lovera et al. 2019). However, considering that the plants in this study inhabit a wash, they may be tapping deep, relatively stable conservation.

Green stems are considered part of a key suite of drought-survival traits (Pivovaroff et al. 2016; Santiago et al. 2016). The ability of stems to photosynthesize after leaf loss may promote plant carbon balance and prolong survival during drought. Besides this possible advantage of green stems, little is known about their water cost compared to non-green stems. Most green-stemmed species keep their young epidermis, which is less resistant to water loss than non-green bark tissue. In other words, during drought a green-stemmed plant might continue to lose water through their outer layer even if all stomata are closed, whereas, non-green stemmed species develop a waterproof layer in their stem that limits their water loss. Our main objective was to compare carbon dioxide uptake and loss of water vapor between leaves and stems of green- and non-green-stemmed species. Normally, non-green stems only lose carbon dioxide to the atmosphere through respiration, whereas green stems can either take up carbon dioxide from the atmosphere in a process known as stem net photosynthesis (SNP) or re-assimilate internally respired carbon dioxide in a water sources throughout the year.

Models that predict drought-induced plant mortality are needed to predict the relative vulnerability of these plant types and to better understand the mechanisms behind physiological responses to changes in climate. Multiple models have been used for simulating physiology of plants in order to predict mortality (McDowell et al. 2013). However, none of these models have accounted for the extra carbon income derived from stem photosynthesis, which could prolong survival during drought. Our work increased our knowledge of the physiology of desert green-stemmed species and their possible responses to climate change by showing the greater water loss of green stems. In addition, studying the costs and benefits of green stems in other ecosystems will increase our understanding of the way plants cope with drought, and help to predict which plants might die first. If species with green stems can maintain photosynthetic carbon dioxide uptake during drought, even at a low rate, they would not be as likely to die of carbon starvation. However, if species with green stems also lose substantially more water through their epidermis during drought, they might be at an increased risk of hydraulic failure. Finally, models used so far can be re-parameterized to account for stem carbon dioxide assimilation and to test if carbon starvation, hydraulic failure, or both mechanisms are responsible for mortality of green-stemmed plants.

Future Directions

The results of this study can be used in screening programs to select species that are better adapted to face more intense, longer and more frequent droughts, which are the predictions of climate change in our desert and Mediterranean climate ecosystems. These plants can be successfully used in restoration practices of degraded arid lands, as it has been done in a tropical semi-arid ecosystem (Fajardo et al. 2013). Also, many of the plant species in Joshua Tree National Park are native to California, and their conservation and the management of the land they occupy is essential if we want to preserve its great biodiversity.

References

• Ávila E, Herrera A, Tezara W (2014) Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. 52:3–15
• Ávila-Lovera E, Haro R, Ezcurra E, Santiago LS (2019) Costs and benefits of photosynthetic stems in desert species from southern California. Functional Plant Biology 12.
• Chaves MM, Pereira JS (1992) Water stress, CO2 and climate change. Journal of Experimental Botany 43:1131–1139.
• Chaves MM, Pereira JS, Maroco J, et al (2002) How plants cope with water stress in the field? Photosynthesis and growth. Annals of Botany 89:907–916.
• Ehleringer JR, Comstock JP, Cooper TA (1987) Leaf-twig carbon isotope ratio differences in photosynthetic-twig desert shrubs. Oecologia 71:318–320
• Fajardo L, Rodríguez JP, González V, Briceño-Linares JM (2013) Restoration of a degraded tropical dry forest in Macanao, Venezuela. Journal of Arid Environments 88:236–243.
• Gibson AC (1996) Structure-function relations of warm desert plants. Springer Berlin Heidelberg, Berlin, Heidelberg
• Lambers H, Chapin FS, Pons TL (2008) Plant Physiological Ecology. Springer New York, New York, NY
• McDowell N, Pockman WT, Allen CD, et al (2008) Mechanisms of plant survival and mortality during drought: Why do some plants survive while others succumb to drought? New Phytologist 178:719–739.
• McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiology 155:1051–1059. https://doi.org/10.1104/pp.110.170704
• McDowell NG, Beerling DJ, Breshears DD, et al (2011) The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution 26:523–532.
• McDowell NG, Fisher RA, Xu C, et al (2013) Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework. New Phytologist 200:304–321.
• Nilsen E, Sharifi M (1997) Carbon isotopic composition of legumes with photosynthetic stems from Mediterranean and desert habitats. American Journal of Botany 84:1707–1713
• Nilsen ET (1995) Stem photosynthesis: extent, patterns, and role in plant carbon economy. In: Gartner BL (ed) Plant stems: physiology and functional morphology. Academic Press, San Diego, pp 223–240
• Nilsen ET, Bao Y (1990) The influence of water stress on stem and leaf photosynthesis in Glycine max and Sparteum junceum (Leguminosae). American Journal of Botany 77:1007–1015.
• Osmond CB, Smith SD, Gui-Ying B, Sharkey TD (1987) Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Characterization of leaf and stem CO2 fixation and H2O vapor exchange under controlled conditions. Oecologia 72:542–549
• Pivovaroff AL, Pasquini SC, De Guzman ME, et al (2016) Multiple strategies for drought survival among woody plant species. Functional Ecology 30:517–526.
• Santiago LS, Bonal D, De Guzman ME, Ávila-Lovera E (2016) Drought survival strategies of tropical trees. In: Goldstein G, Santiago LS (eds) Tropical Tree Physiology. Springer International Publishing, Cham, pp 243–258
• Schaedle M (1975) Tree Photosynthesis. Annual Review of Plant Physiology 26:101–115.
• Sevanto S, Mcdowell NG, Dickman LT, et al (2014) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses. Plant, Cell & Environment 37:153–161.
• Smith SD, Osmond CB (1987) Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Morphology, stomatal conductance and water-use efficiency in field populations. Oecologia 72:533–541
• Tinoco-Ojanguren C (2008) Diurnal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert. Journal of Arid Environments 72:127–140.

Biography

Dr. Eleinis Ávila-Lovera is a plant ecophysiologist interested in understanding the process and advantages of stem photosynthesis. Her research focuses on studying plants from arid and semi-arid ecosystems in southern California and the Tropics, where green stems are advantageous. She has found that stem photosynthesis is very similar to leaf photosynthesis and that plants bearing green stems can continue assimilating carbon during the dry season, when most plants in deserts are leafless.