Plants that live on air

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plantes azote - azote - fixation azote plantes

Use nitrogen from the air to synthesize its essential biomolecules? Plants achieve this feat by establishing a mutually beneficial association with soil bacteria. After a specific recognition process, the partners establish a symbiosis. Bacteria enter the root and the cortex cells divide. A specific organ is then formed, the nodule, in which atmospheric nitrogen from the air is used for the synthesis of amino acids that are then used to form proteins. This association has major economic and environmental advantages. This makes the use of nitrogen fertilizers virtually unnecessary and reduces air and groundwater pollution. These plants that live on the air of the times also have important nutritional qualities and are therefore particularly interesting.

1. Nitrogen, a plant growth limiting factor

Nitrogen (N), like carbon (C), hydrogen (H) and oxygen (O), is an essential component of life and ecosystems. It is essential to life because it is involved in the constitution of many biomolecules such as proteins, nucleic acids, nucleotides or chlorophyll. Reactive nitrogen, which can be used by plants, is present in the soil mainly in the form of nitrate (NO3) and ammonia (NH3).

plants tomates - azote plantes
Figure 1. Effects of nitrogen deficiency on plant growth. 4-week-old tomato plants grown in the presence of 0, 10, 30 and 100% of the plant’s nitrogen requirements [Source: © Renaud Brouquisse].
The distribution of plants on the surface of the globe is uneven: it is denser in temperate and tropical regions, and more sparse in polar and desert regions. This is due to the fact that plant development is limited by many environmental factors. After water availability, reactive nitrogen availability* is the second limiting factor for plant growth (Figure 1). This is why world agriculture uses large amounts of nitrogen fertilizers.

Plants obtain the nitrogen they need by absorbing it from the roots in the form of NO3 or NH3. But some species are also able to establish a relationship with marine or terrestrial bacteria that can use nitrogen from the air: this is the biological nitrogen fixation.

2. The plant – nitrogen-fixing bacteria relationship

2.1. The variety of nitrogen-fixing organisms

fixateurs biologiques azote - azote - azote plantes
Figure 2. Biological nitrogen fixers. A, Marine filamentous cyanobacteria; B, Sea Buckthorn, in symbiosis with actinomycete Frankia. [Source: A, © Jean-Claude Druart, INRA Media Library; B, Vmenkov (GFDL or CC BY-SA 4.0), via Wikimedia Commons]
Biological fixation of atmospheric nitrogen is only achieved by bacteria. Three categories of nitrogen-fixing bacteria can be distinguished:

  • Marine cyanobacteria, including filamentous cyanobacteria living in colonies (Trichodesmium, …), and unicellular cyanobacteria living either free or in symbiosis with phytoplankton (Nostoc, Anabaena,…; Figure 2). They are responsible for 40 to 50% of biological nitrogen fixation.
  • Free soil bacteria, some of which are aerobic (Azomonas, Azotobacter,…) and others anaerobic (Desulfovibrio, Clostridium,…). Some are called phototrophic because they derive their energy source from light (Chromatium, Chlorobium,…), others are called chemotrophic because they use the energy of the oxidation of mineral compounds (chemo-lithotrophic: Thiobacillus, Methanococcus,…) or organic (chemo-organotrophic: Methylomonas, Azotobacter,…). They are said to be responsible for 5 to 10% of biological nitrogen fixation.
  • The third category, the one of interest here, includes soil bacteria that live in symbiosis* with the root system of plants (see Symbiosis & parasitism). These are the actinomycete Frankia, which establishes symbioses with various angiosperms species (alder, sea buckthorn, Casuarinaceae; Figure 2) and Rhizobium-type bacteria that enter into symbiosis with plants of the legume family (Fabaceae) [1]. This family, which includes about 18,000 species (soybean, alfalfa, bean, lentil, groundnut, licorice, clover, wisteria, mimosa,…), is characterized by papilionaceous flowers (butterfly-shaped), a pod (fruit from the flower’s ovary) containing seeds and, for the majority of its members, the ability to use atmospheric nitrogen to produce its own nitrogen components through symbiosis with Rhizobia. [1]

2.2. How do the two partners recognize each other?

Figure 3. Mutual recognition process between a legume (alfalfa) and a bacterium of the Rhizobium type (Sinorhizobium meliloti). [Source: © Renaud Brouquisse & Alain Puppo]
It is through the mutual recognition of the two partners (the plant and the bacteria) that the symbiotic process begins. In response to the secretion of flavonoids* by the root (Figure 3), bacteria are attracted to it and synthesize lipo-chito-oligosaccharides*, called nod factors (for nodulation). This process is characterized by a high specificity: Rhizobia recognized by soybean will not be recognized by alfalfa and vice versa.

2.3. Nodules formation

Figure 4. Diagram of the establishment, formation and structure of an indeterminately growing nitrogen fixing nodule of the alfalfa type. [Source: © Marc Bosseno, INRA Media Library]
At the root surface, under the influence of nod factors, bacteria attach themselves to the root  hair whose end curves into a “shepherd’scross” in which microsymbiotes* gather (Figure 4). Root infection is initiated by invagination of the plasma membrane of the cell constituting the root  hair. A tubular structure, called an infection thread, contains bacteria that progress to the root cortex*.

Nod factors also trigger the de-differentiation (divisional entry) of cells from the  root cortex, leading to the creation of a meristem* at the origin of a new organ: the nodule (Figure 4). This is gradually invaded by symbiotic bacteria, now called bacteroids. However, they are not free in the plant cells; they are surrounded by a membrane of plant origin, the peribacteroidal membrane, which will regulate exchanges between the two partners (Figure 5).

Figure 5. Exploded view and detail of an alfalfa nodule (Medicago sativa), photo credit INRA. Refer to Figure 5 and text for the numbers of zones I to IV. [Source: © Renaud Brouquisse & Alain Puppo]
Some nodules, with undeterminate growth, retain a meristem and their structure can be divided into several zones (Figures 4 and 5) [2]: the division zone (I) where the cells divide and nodule increases; the infection zone (II) where bacteria enter the plant cells and transform into bacteroids; the fixation zone (III) where atmospheric nitrogen (N2) is reduced to ammonia (NH3) by bacterial nitrogenase; the senescence zone (IV) where the bacteroids, then the plant cells die.

2.4. Nodule: a haven for bacteroids

Within the nodule, the oxygen concentration is strongly reduced compared to the atmospheric content. These microaerophilic* conditions allow the enzyme responsible for nitrogen fixation, bacterial nitrogenase, to be active. This enzyme is inactivated by oxygen. These conditions are allowed by the combination of two processes:

  • On the one hand, a gas diffusion barrier is established in the nodule cortex thanks to layers of cells without intercellular space;
  • On the other hand, infected plant cells contain a haemoprotein with a high affinity for oxygen: the leghaemoglobin.This protein, which is red in colour and has a structure comparable to animal myoglobin, provides oxygen to bacteroids at concentrations low enough not to inactivate nitrogenase.

Figure 6. Carbon-nitrogen exchanges between the plant cell and the bacteroid in a nodule. [Source: © Renaud Brouquisse & Alain Puppo]
In the functioning of symbiosis, the plant supplies the microbial partners with carbon-containing nutrients (organic acids), to feed their energy metabolism; in exchange, the bacteroids provide the plant with ammonia (NH3/NH4+) which is incorporated into the plant proteins (Figure 6). The expression “living from the air of the times” thus takes on its full meaning, since the plant is able to draw from the atmosphere the carbon (via photosynthesis) and nitrogen (via biological fixation) it needs for the synthesis of its biomolecules.

It is important to note that when the legume grows on soil naturally rich in nitrate or ammonia, it uses the latter as a source of nitrogen. The symbiotic process is then inhibited and symbiosis does not take place.

3. Symbiotic association, a major advantage for ecosystems and agronomy

Figure 7. Nitrogen cycle diagram.

Nitrogen permanently exits and enters the soil through the nitrogen cycle (Figure 7). There are three main ways in:

  • Recycling of decomposing organic matter (Step 4) [3]. Humus, derived from dead plants, crop residues and livestock manure, supplies soil and aquatic environments with organic matter (Step 1). In well oxygenated soils and aquatic environments, bacteria convert ammonia into nitrite (NO2) and then nitrate (NO3) during the nitrification process (Step 5).
  • The spreading of fertilizers and nitrogen fertilizers (Step 5). These have been produced for more than 80 years by the Haber-Bosch chemical process [4] (Figure 8), which is used to synthesize ammonia by hydrogenation of atmospheric gaseous dinitrogen by gaseous hydrogen (H2) in the presence of a catalyst (Step 3). They now represent the main contribution of nitrogen to agriculture in industrialized countries in North and South America, Europe and Australia, and their use has increased significantly in recent decades (Figure 8).
  • The biological nitrogen fixation we have described, in particular via the symbiosis between Rhizobia and legumes (Step 2). The latter, cultivated for at least 12,000 years around the Mediterranean basin, have for centuries played an essential role in the regeneration of agricultural land for nitrogen through the three-year crop rotation (a fallow year, a legume year, a cereal year). Today, biological nitrogen fixation is estimated at between 150 and 250 million tonnes per year, including about 50 million tonnes from legumes in symbiosis; by comparison, industrial production of nitrogen fertilizers by the Haber-Bosch process represents about 100 million tonnes per year [5].

Figure 8. Haber-Bosch process for the manufacture of chemical fertilizers (A) and the contribution of chemical fertilizers to food production and human population since the beginning of the 20th century (B). [Source: © Renaud Brouquisse & Alain Puppo]
The amount of nitrogen contained in a soil and bound to carbon (97 to 99% of total nitrogen) varies from 2 to 10 tonnes per hectare. Nitric and ammoniacal fractions, available and used for plant growth, represent only 1 to 3% of total nitrogen. Nitrogen is removed from the soil in three types of processes:

  • Through their roots, plants absorb nitrate and ammonia from the soil and incorporate them into amino acids, proteins and all nitrogen molecules necessary for their growth (Step 10).
  • Plants are then a primary source of available nitrogen for herbivorous animals, including humans, to consume (Steps 9 & 11).
  • In poorly oxygenated soils or aquatic environments, so-called “denitrifying” bacteria transform ammonia and nitrate into N2 which can be returned to the atmosphere via a denitrification process (nitrate, NO3, to dinitrogen, N2, reduction process) (Step 7).

However, not all the nitrogen in the soil is assimilated or transformed into nitrogen. A significant part, which varies according to the nature and content of the soil in nitrogen compounds, is:

  • either carried to groundwater by runoff (referred to as leaching) (Step 6),
  • or volatilized into the atmosphere as ammonia or nitrogen oxides (NOx: mainly NO and NO2) (Step 8).

These losses constitute a nitrogen depletion of the soil and a source of pollution of the atmosphere and groundwater (see Nitrates in the environment).

Over the past 100 years or so, through the increase in industrial activities and the massive use of nitrogen fertilizers, human activities have significantly altered the nitrogen cycle. Today, the risk of saturation of the planet with reactive nitrogen is real and its implications for ecosystems are still poorly assessed.

4. Interest of legumes for food and the environment

4.1. A food source and a nutritional asset

legumineuses
Figure 9. Food legumes. From left to right and top to bottom: green bean (Phaseolus vulgaris), lupin (Lupinus albus), faba bean (Vicia faba), brown lens (Lens culinaris), faba bean (Vicia faba), red bean (Phaseolus vulgaris), coral lens (Lens culinaris), pea (Pisum sativum), chickpea (Cicer arietinum). [Source: © Jean-Marie Bossennec, © Roland Bruneau, © Chantal Nicolas, © Christophe Maitre, © Gérard Duc, © Renaud Brouquisse, © Jean Weber, all from the INRA Media Library]
Legumes have important qualities for human and animal nutrition [6]. Protein-rich fodder legumes are used to feed animals either by grazing or after fodder storage (hay, silage, dehydration). Seed legumes are used for animal and human food (Figure 9). They are particularly rich in protein, which accounts for 20 to 40% of their dry weight. In comparison, proteins represent only 6 to 13% of the dry weight of cereals. In addition, legume proteins contain essential amino acids that humans are not able to synthesize and must find in their diet. They are rich in lysine, but low in sulphur-containing amino acids (methionine, cysteine), while cereal proteins are rich in methionine and cysteine, but low in lysine. Legumes are therefore an excellent complement to cereals for a balanced diet of plant proteins [7].

In most edible legume species, the fat content of the seeds is low (1-10% of dry weight), but there are exceptions and in some species referred to as oilseeds, the seeds may contain 20% (soybean) and up to 50% (peanut) of their dry weight in fat.

While carbohydrate levels vary widely among legumes (20 to 65% of dry weight), their glycemic index* is generally low; moreover, they essentially contain a form of starch (amylose) that the body digests slowly and causes little variation in blood sugar. In addition, soluble and insoluble fibres present in seeds have a beneficial effect on digestive tract health and digestion; on the other hand, some fermentable fibres (a-galactosides) can cause risks of flatulence.

Legume seeds are also rich in vitamins (B1, B2, B3, E) and minerals (potassium, phosphorus, magnesium, zinc, iron, manganese, calcium, etc.). However, in dry seeds, the bioavailability of these compounds is reduced by the presence of anti-nutritional factors, such as protease and amylase inhibitors, or secondary metabolites such as phytates or tannins [8]. Most of these anti-nutritional factors are destroyed or inactivated by hydrothermal treatments (seed soaking and cooking), which increases the bioavailability of the various seed components.

Because of their good digestibility (80 to 90% after soaking and cooking), legume proteins can be compared to animal proteins and provide an alternative to meat consumption [2]. In terms of health and well-being, the nutritional intakes of legumes therefore have their rightful place in a varied and balanced diet. Their consumption makes it possible to better prevent cardiovascular diseases, as well as the risks of type 2 diabetes, obesity and certain cancers (colorectal, breast) [4]. A minor drawback, however, is that soybeans and especially groundnuts are highly allergenic legumes whose consumption can sometimes lead to food allergies.

4.2. A source of nitrogen and an environmental asset

Because of the symbiosis with nitrogen-fixing bacteria, legumes are therefore a natural fertilizer. They were among the first plant species domesticated in the fertile crescent more than 12,000 years ago. At the death of the plant, during the degradation of the root and aerial parts, the mineralization of organic matter releases nitrogen in forms (nitrate, ammonia, amino acids) that are easily assimilated by neighbouring plant species or subsequent crops. Today, legume cultivation accounts for about 25% of the nitrogen input to cultivated areas (about 20% in European and North American countries, and more than 50% in Asia, Africa and South America), with industrial fertilizers accounting for 63% and combustion processes for 13% [9]. The cultivation of legumes has a major environmental impact because:

  • Because they require little or no fertilization, they allow a significant saving in fertilizers whose manufacturing cost is high (it takes the equivalent of 2 tons of oil to produce 1 ton of nitrogen fertilizer by the Haber-Bosch process).
  • Reducing the use of fertilizers reduces groundwater pollution by reducing leaching*, which in turn reduces eutrophication*;
  • They have a positive effect on the balance of greenhouse gas (GHG) emissions, including CO2, N2O or ammonia, which are mainly derived from mineral fertilizers and animal waste (symbiotic fixation produces only a small amount of N2O).

To these advantages, directly linked to the existence of symbiosis, are added those inherent to legumes, whether or not they establish a symbiosis with Rhizobium:

  • They improve, by also being able to establish a mycorrhizal symbiosis, the removal of phosphorus from the soil (another factor limiting plant growth), and make it more available to other plant species.
  • They have a positive impact on the soil (stabilization, limitation of runoff and erosion through the development of their root system) and a positive effect on crop rotations (reduction in fertilizer use, reduction in plant protection treatments).
  • Finally, as a natural fertilizer, they have a positive effect on biodiversity by increasing the productivity of plant species, promoting pollinators (bees) and providing refuges for crop auxiliaries and macrofauna (birds, mammals).

5. Crop associations, a solution for agro-ecology

Figure 10. Associated cultures. A, left: Alternate cereal-vetch cultivation; B, center: Organic mixed cereal (triticale; barley; oats) and legumes (peas) cultivation; C, right: Simple agroforestry system combining one perennial woody species in row (olive tree) and two species in culture, under the row, cover or nitrogen fixing plant (alfalfa) and inter row, food plant (durum wheat). [Source: A, Michel Gosselin INRA Media Library; B and C, Christophe Maître, INRA Media Library]
In large-scale farming regions, French agriculture is strongly influenced by the simplification of crop rotation and the increased use of inputs (fertilizers). Diversified agro-ecosystems are increasingly recognized as a crucial lever for sustainable development. The increase in diversity cultivated within the plot was specifically tested through cereal – legume associations, sown and harvested together (Figure 10). It appears that these associations make it possible to meet the challenges of production, reduction of inputs and environmental impacts of crops and stability in the face of biotic and abiotic hazards in both organic and conventional agriculture [10]. The selection of varieties well adapted to these crop associations is becoming a major challenge in this context.

Associated crops* cereal – legume improve resource utilization compared to a single crop. This leads in particular to:

  • a better grain/seed yield* than the average yield of each single crop,
  • a reduction in weed biomass compared to growing legumes alone,
  • and a higher protein concentration in the grains of the cereal compared to the cultivation of the cereal alone.

The advantages of the associated crop are all the more marked when the conditions are unfavourable: low yield of each crop or both grown separately or low protein content of the grain of the cereal grown alone. Associated crops are particularly beneficial when nitrogen is limiting for crops and helps to stabilize yields in organic agriculture.

The achievement of these benefits is closely linked to the proportion of legumes within the association. Thus, in grasslands, the optimal operating conditions are about 30 to 40% fodder legumes for grazed associations and 50 to 70% for mowing associations. In any case, legumes can thus be a driving force for reorienting crops towards sustainable agriculture that respects the ecological, economic and social standards that ensure that agricultural production is maintained over time.

6. Messages to remember

  • Some bacteria are able to use atmospheric nitrogen for the synthesis of their biomolecules (marine cyanobacteria, soil bacteria that are free or in symbiosis with the roots of certain plants): this is the biological fixation of nitrogen.
  • In the case of legumes, symbiotic bacteria penetrate the root system and cause the formation of a new organ: the nodosity. This organ is the place where atmospheric nitrogen is reduced to ammonia; it contains a protein comparable to animal myoglobin: leghaemoglobin.
  • Legumes are high in protein and are an excellent complement to cereal protein for a balanced vegetable protein diet.
  • The benefits of biological nitrogen fixation are multiple: economic (nitrogen fertilizer savings) and environmental (reduced air and groundwater pollution, crop associations for sustainable development).

 


References and notes

Cover image. [Source: © Marie-Christine Lhopital, INRA Media Library]

[1] Vegetables and legumes should not be confused. Vegetable comes from the Latin legumen which referred to plants whose fruit is a pod (pod of “legumes”). Subsequently, legumen has designated all vegetable plant species and, in its current use, a vegetable is a cultivated plant whose consumption depends on the species, leaves, roots, tubers, fruits, seeds; vegetable also refers to the consumed part of this plant. Note that in French, legumes are called “légimineuses”.

[2] Ferguson BJ, Indrasumunar A, Hayashi S, Lin M-H, Lin Y-H, Reid DE, Gresshoff PM (2010). Molecular analysis of vegetable nodule development and autoregulation. Journal of Integrative Plant Biology, 52: 61-76.

[3] The numbers in brackets refer to the nitrogen cycle diagram (Figure 7).

[4] The Haber-Bosch process makes it possible to economically fix atmospheric nitrogen in the form of ammonia, which in turn allows the synthesis of different explosives and nitrogen fertilizers. As such, from a demographic point of view, it is probably the most important industrial process ever developed during the 20th century.

[5] Erisman E, Sutton MA, Galloway J, Klimont Z, Winiwarter W (2008). How a century of ammonia synthesis changed the world. Nature Geoscience, 1: 636-639.

[6] Champ M, Magrini M-B, Simon N, Le Guillou C (2015). Les légumineuses pour l’alimentation humaines : apport nutritionnel et effets santé, usages et perspectives. In Les légumineuses pour des systèmes agricole et alimentaires durables, Schneider A & Huyghe C Coord., Editions Quae, pp 263-295. (in french)

[7] Tomé D (2012). Criteria and markers for protein quality assessment – a review. Brit. J. Nutr. 108 (S2): S222-229.

[8] Champ M, Anderson JW, Bach-Knudsen KE (2002). Supplement pulses and human health. Brit. J. Nutr, 88 (S3):S237-319.

[9] Cellier P, Schneider A, Thiébeau, Vertès F (2015). Impact environnementaux de l’introduction des légumineuses dans les systèmes de production. In Les légumineuses pour des systèmes agricoles et alimentaires durables, Schneider A & Huyghe C Coord., Editions Quae, pp 297-338. (in french)

[10] Corre-Hellou G et al. (2013). Associations céréale-légumineuse multi-services. Innovations Agronomiques 30, 41-57. (in french)


The Encyclopedia of the Environment by the Association des Encyclopédies de l'Environnement et de l'Énergie (www.a3e.fr), contractually linked to the University of Grenoble Alpes and Grenoble INP, and sponsored by the French Academy of Sciences.

To cite this article: BROUQUISSE Renaud, PUPPO Alain (August 16, 2019), Plants that live on air, Encyclopedia of the Environment, Accessed November 1, 2024 [online ISSN 2555-0950] url : https://www.encyclopedie-environnement.org/en/life/plants-that-live-on-air/.

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靠空气生存的植物

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plantes azote - azote - fixation azote plantes

  利用空气中的氮能合成基本的生物分子吗?植物能够通过与土壤细菌建立一种互惠互利的关系来实现这一目标。通过一种特定的识别过程,合作伙伴之间建立了一种共生关系。细菌进入根部,皮层细胞分裂。然后形成一个特定的器官,即根瘤,在根瘤中,空气中的氮合成氨基酸,氨基酸再形成蛋白质。这种关系具有重大的经济和环境优势。如此一来就几乎没有必要施用氮肥,并减少了空气和地下水污染。这些靠当下的空气生存的植物还具有重要的营养价值,因此特别引人关注。

1. 氮,植物生长限制因子

  氮(N)与碳(C)、氢(H)和氧(O)一样,是生命和生态系统的重要组成部分。它是生命所必需的,因其参与了许多生物分子的组成,如蛋白质、核酸、核苷酸或叶绿素。活性氮主要以硝态氮(NO3-)和氨态氮(NH3)的形式存在于土壤中,可被植物利用。

环境百科全书-靠空气生存的植物-缺氮对植物生长的影响
图1. 缺氮对植物生长的影响。在满足0、10%、30%和100%的植物氮需求量的条件下生长的4周龄番茄植株 [来源:© Renaud Brouquisse]。

  植物在地球表面的分布是不均衡的:在温带和热带地区较为密集,在极地和沙漠地区则较为稀疏。这是由于植物的生长发育受到许多环境因子的限制。除水源外,活性氮*是植物生长的第二大限制因子(图1)。也是因为此,氮肥在世界农业中被大量使用。。

  植物从根部以NO3-或NH3的形式吸收所需的氮。然而,一些物种也能够与海洋或陆生细菌建立联系,这些细菌可以利用空气中的氮:这就是生物固氮。

2. 植物-固氮菌的关系

2.1. 固氮生物的种类

环境百科全书-靠空气生存的植物-生物固氮细菌
图2. 生物固氮细菌 A 海洋丝状蓝藻; B 沙棘与弗兰克放线菌的共生关系
[来源: A,©Jean-Claude Druart, 法国国家农业科学研究院媒体图书馆; B, Vmenkov (GFDL或CC BY-SA 4.0),通过Wikimedia Commons]

  大气中氮的生物固定只能通过细菌来实现。固氮细菌可分为三类:

  • 海洋蓝藻,包括生活在菌落中的丝状蓝藻 (束毛藻属),游离或与浮游植物共生的单细胞蓝蓝藻(念珠藻属,鱼腥藻属等;图2)。它们占生物固氮量的40-50%。
  • 游离土壤细菌,有些是好氧的(氮单胞菌属、固氮菌等),有些是厌氧的(脱硫弧菌属,梭菌属等)。有些被称为光养型,因为它们的能量来源是光(着色菌属,绿菌属等)。另一些则被称为化学营养型,因为它们利用矿物化合物氧化的能量(无机化能营养的:硫杆菌,甲烷球菌属)或有机化合物(有机化能营养的:甲基单胞菌属,固氮菌等)。它们占生物固氮量的5-10%。
  • 第三类,这是我们感兴趣的,包括与植物根系共生的土壤细菌*(参见“共生与寄生”)。如弗兰克氏菌属的放线菌,它与各种被子植物( 桤木,沙棘,木麻黄科;图2)和与豆科植物(豆科)共生的根瘤菌类细菌建立了共生关系[1]。该科包括约18000种(大豆,苜蓿,菜豆,小扁豆,落花生,甘草,三叶草,紫藤,含羞草等),特征是蝶形花(蝴蝶状),含有种子的豆荚(花子房的果实),其大多数成员能够通过与根瘤菌的共生利用大气中的氮来产生自己的氮成分。

2.2. 双方如何相互识别?

环境百科全书-靠空气生存的植物- 科植物与根瘤菌的相互识别过程。
图3. 豆科植物(苜蓿)与根瘤菌(苜蓿中华根瘤菌)的相互识别过程
[来源: ©Renaud Brouquisse & Alain Puppo](图3 Host plant 宿主植物,alfalfa 苜蓿,Nod factors 结瘤因子,Flavonoids 类黄酮,Sinorhizobium meliloti 苜蓿中华根瘤菌)

  正是通过这两者(植物和细菌)的相互识别,共生过程才开始。为了响应根分泌的类黄酮*(图3),细菌被吸引到根上并合成脂壳寡糖*,又称结瘤因子(用于结瘤)。该过程具有高度特异性:大豆识别的根瘤菌不能被苜蓿识别,反之亦然。

2.3. 结瘤形成

环境百科全书-靠空气生存的植物-苜蓿型不定型生长固氮根瘤的建立、形成和结构
图4. 苜蓿型不定型生长固氮根瘤的建立、形成和结构示意图。[来源:©Marc Bosseno, 法国国家农业科学研究院媒体图书馆](图4 Rhizobium 根瘤菌,Root hair 根毛,Infection thread 侵染线,Nodule primordium 根瘤原基,Ⅰ-Divison Ⅰ-分裂区,Ⅱ-Infection Ⅱ-侵染区,Ⅲ-N2 Fixation Ⅲ-固氮区,Ⅳ-Senescence Ⅳ-衰老区,Epiderm 表皮,Cortex 皮层,Endoderm 内皮层,Vascular bundle 维管束)

  在根表面,受结瘤因子的影响,细菌附着在根毛上,根毛的末端弯曲成“牧羊人十字形”,微共生体*在其中聚集(图4)。根侵染是由组成根毛的细胞质膜内陷引起的。侵染线(一种管状结构)包含进入到根皮层*的细菌。

  结瘤因子还触发细胞从根皮层去分化(分裂进入),导致在新器官的起源处产生分生组织*:根瘤(图4)。它逐渐被共生细菌(现在称之为类菌体)入侵。然而,它们在植物细胞中并不是游离的;而是被一层植物膜所包围,这层膜叫做类菌体周膜,它会调节两个共生体之间的交换(图5)。

环境百科全书-靠空气生存的植物-苜蓿结瘤的解剖和细节
图5. 苜蓿结瘤的解剖和细节图(紫花苜蓿),图片来源法国国家农业科学研究院。参见图5和I-IV区编号的文本。[来源:©Renaud Brouquisse & Alain Puppo](图5 Alfalfa 苜蓿,Bacterois 类菌体,Peribacteroid membrane 类菌体周膜,Plant cell 植物细胞,Roots nodules 根瘤,Nodules 结瘤)

  有些无限生长的根瘤保留有分生组织,其结构可分为几个区(图4和图5)[2]: 细胞分裂和结节增加的分裂区(I);细菌进入植物细胞并转化为类菌体的侵染区(II);细菌固氮酶将大气氮(N2)还原为氨(NH3)的固氮区(III); 类菌体,植物细胞死亡的衰老区(IV)。

2.4. 结瘤:类菌体的天堂

  在结瘤内,氧浓度远低于大气中的含量。这些微需氧*条件使负责固氮的酶(细菌固氮酶)具有活性。这种酶会被氧灭活。这些条件可以通过两个过程的结合来实现:

  • 一方面,由于细胞层没有细胞间隙,结瘤皮层内形成了气体扩散屏障;
  • 另一方面,受感染的植物细胞含有一种对氧气有高亲和力的血蛋白:豆血红蛋白。这种蛋白质呈红色,其结构类似于动物肌红蛋白,能以足够低的浓度为类菌体提供氧气,同时不会使固氮酶失活。
环境百科全书-靠空气生存的植物-植物细胞与类菌体在结瘤中的碳氮交换
图6. 植物细胞与类菌体在结瘤中的碳氮交换。[来源:©Renaud Brouquisse & Alain Puppo](图6 C Import 碳输入,N Export 氮输出,Vascular system维管系,Sugars 糖,Amino acids 氨基酸,Organic acids 有机酸,Bcateroid 类细菌,Nitrogenase 固氮酶,Energy and carbon metabolism 能量与碳代谢,Plant cell 植物细胞)

  在共生功能中,植物为微生物伙伴提供含碳的营养物质(有机酸),以促进它们的能量代谢;作为交换,类菌体为植物提供氨(NH3/NH4+),与植物蛋白结合(图6)。因为植物能够从大气中吸收合成其生物分子所需的碳(通过光合作用)和氮(通过生物固定),所以“依靠当下的空气生活”这一表述具有完全的意义。

  值得注意的是,当豆科植物在天然富含硝酸盐或氨的土壤生长时,它会使用后者作为氮源。共生过程就会遭到抑制,不再发生。

3. 共生关系是生态系统和农学的主要优势

环境百科全书-靠空气生存的植物-氮循环图
图7 氮循环图。(图7 Deposition 沉积,Nitrogen-fixing bacterias 固氮细菌,NH3 synthesis 氨合成,Mineral Nitrogen-containing fertilizers 矿物含氮肥料,Organic Nitrogen 有机氮,Biological activity生物活性,Organisation 组织,mineralisation 矿化,Humus 腐殖质,Labile organic matter 活性有机质,Mineral Nitrogen 矿质氮,Urea 尿素,Ammoniac NH3 氨,nitrification 硝化作用,Nitrate NO3- 硝酸盐,Lixivation 浸出,Denitrification 反硝化作用,Animal manure畜肥,Plant residues 植物残体, Volatilization 挥发,Atmospheric Nitrogen N2 大气氮N2,Export 输出,Food 食物,Loss of Nitrogen from the soil 从土壤中流失氮,Input of Nitrogen to the soil 向土壤中输入氮,Transfer to water or air 转移到水或空气中)

  氮通过氮循环永久退出并进入土壤(图7)。主要有三种途径:

  • 分解有机物的回收(步骤4)[3]。腐殖质来源于死亡的植物,作物残茬和牲畜粪便,为土壤和水生环境提供有机物(步骤1)。在氧化良好的土壤和水环境中,细菌在硝化过程中将氨转化为亚硝酸盐(NO2-)和硝酸盐(NO3-)(步骤5)。
  • 施肥和施氮肥(步骤5)。肥料和氮肥已经通过哈伯-博施化学工艺生产了80多年(图8),该工艺用于在催化剂存在下,用气态氢(H2)使大气气态二氮加氢合成氨(步骤3)。肥料和氮肥现在是北美、南美、欧洲和澳大利亚等工业化国家农业氮的主要来源,近几十年来它们的用量显著增加(图8)。
  • 上文提到的生物固氮,特别是通过根瘤菌和豆科植物之间的共生(步骤2)所形成的。豆科植物在地中海盆地种植了至少12000年,几个世纪以来,通过三年的轮作(休耕年,豆类年,谷物年),在农业用地的氮再生方面发挥了重要作用。今天,生物固氮估计每年在1.5亿至2.5亿吨之间,其中约5000万吨来自共生的豆科植物;相比之下,通过哈伯-博施工艺生产的氮肥工业产量约为每年1亿吨[5]
环境百科全书-靠空气生存的植物-制造化肥的哈伯-博施法
图8 制造化肥的哈伯-博施法(A)和20世纪初以来化肥对粮食生产和人口的贡献(B)。[来源:©Renaud Brouquisse & Alain Puppo]
(图8 A Industrial nitrogen reduction (Haber-Bosch process)工业氮还原反应(哈伯-博施法),图8 B World population 世界人口,World population fed by Haber Bosch nitrogen靠哈伯-博施法制氮养活的世界人口,Average fertilizer input平均化肥输入,World population average fertilizer input 世界人口平均化肥输入)

  土壤中含氮量和与碳(总氮的97 – 99%)结合的含氮量不等,约为每公顷2 – 10吨。可用于植物生长的氮和氨组分仅占总氮的1% – 3%。从土壤中除氮的过程有三种:

  • 通过根系,植物从土壤中吸收硝酸盐和氨,并将它们转化为氨基酸、蛋白质和生长所需的所有氮分子(步骤10)。
  • 植物是包括人类在内的草食动物可利用氮的主要来源(步骤9&11 )。
  • 在氧含量低的土壤或水生环境中,所谓的“反硝化”细菌将氨和硝酸盐转化为N2,并通过反硝化过程(硝酸盐,NO3,还原为二氮,N2,还原过程)返回到大气中(步骤7)。

  然而,并非土壤中的所有都被同化或转化为氮。根据土壤性质和氮化物含量的不同,会发生的变化是:

  • 通过径流进入地下水(称为浸出)(步骤6),或以氨或氮氧化物挥发到大气中(NOx:主要是NO和NO2步骤8)。
  • 这些损失构成土壤氮的耗竭,是大气和地下水的污染源(参见“环境中的硝酸盐”)。

  在过去的100多年里,通过工业活动的增加和氮肥的大量使用,人类活动显著地改变了氮循环。今天,地球上活性氮饱和的风险是真实存在的,其对生态系统的影响仍未得到充分的评估。

4. 豆科植物对食物和环境的益处

4.1. 一种食物来源和营养宝库

环境百科全书-靠空气生存的植物-食用豆类
图9 食用豆类。从左到右,从上到下分别为:四季豆(Phaseolus vulgaris),白羽扇豆(Lupinus albus),蚕豆(Vicia faba), 兵豆(Lens culinaris),蚕豆(Vicia faba),菜豆(Phaseolus vulgaris),小扁豆(Lens culinaris),豌豆(Pisum sativum),鹰嘴豆(Cicer arietinum)[资料来源: Jean-Marie Bossennec, Roland Bruneau, Chantal Nicolas, Christophe Maitre, Gérard Duc, ©Renaud Brouquisse, ©Jean Weber, 所有均来自法国国家农业科学研究院媒体图书馆]

  豆科植物对人和动物的营养具有重要的作用[6]。作为富含蛋白质的饲料,豆科植物可以被用于放牧或饲料储存(干草、青贮、脱水)来喂养动物。豆科植物也可作为动物和人类的食物(图9)。它们富含蛋白质,占其干重的20% – 40%。相比之下,蛋白质只占谷物干重的6% – 13%。此外,豆类蛋白质含有人类无法合成,因此得从饮食中获取的必需氨基酸。豆类蛋白质富含赖氨酸,但含硫氨基酸含量较低(蛋氨酸、半胱氨酸);而谷物蛋白质富含蛋氨酸和半胱氨酸,但赖氨酸含量较低。因此,豆类是谷物的绝佳补充,可实现植物蛋白的均衡饮食[7]

  在大多数的可食用豆科植物中,种子的脂肪含量很低(干重的1%-10%),但也有例外,在一些被称为油籽的品种中,种子的脂肪含量可能占其干重的20%(大豆)甚至50%(花生)。

  虽然不同豆科植物的碳水化合物含量差异很大(占其干重的20% – 65%),但它们的血糖指数*通常较低;此外,它们本质上含有一种淀粉(直链淀粉),人体消化缓慢,对血糖的影响很小。此外,种子中的可溶性和不可溶性纤维对消化道健康和消化都有好处;另一方面,一些可发酵纤维(半乳糖苷)可能导致肠胃气胀

  豆类种子还富含维生素(B1、B2、B3、E)和矿物质(钾、磷、镁、锌、铁、锰、钙等)。然而,在干燥的种子中,这些化合物的生物利用率会因抗营养因子(如蛋白酶和淀粉酶抑制剂)或次生代谢物(如植酸盐或单宁)的存在而降低[8]。大多数的抗营养因子被水热处理(种子浸泡和蒸煮)破坏或灭活,从而增加种子各成分的生物利用率。

  由于其良好的消化率(浸泡和烹饪后的80% – 90%),豆类蛋白质可以与动物蛋白质相媲美,提供了肉类消费的替代品[2]。因此,就健康和福祉而言,豆类的营养摄入量在多样化和均衡的饮食中占有一席之地。食用它们可以更好地预防心血管疾病、2型糖尿病、肥胖和某些癌症(结肠直肠癌、乳腺癌)[4]。有点缺憾的是,大豆,尤其花生是高度过敏的豆类,食用它们有时会导致食物过敏。

4.2. 氮的来源与环境价值

  豆科植物与固氮细菌共生,因此是一种天然肥料。它们是12000多年前在新月沃土被家养的首批植物之一。它死亡后,其根部和地上部分在降解过程中,有机质的矿化作用会释放出各种形式的氮(硝酸盐、氨、氨基酸),这些氮很容易就能被邻近的植物物种或后茬作物吸收。如今,在耕地的氮输入中,豆类种植约占25%(欧洲和北美国家约为20%,亚洲、非洲和南美洲超过50%),工业化肥占63%,燃烧过程占13%[9]。豆科植物的种植对环境有重大影响,因为:

  • 它们很少或不需要施肥,可以大大节省较高的肥料生产成本(用哈伯-博施法生产1吨氮肥需要消耗相当于2吨石油)。
  • 减少化肥的使用可以通过减少浸出*来减少地下水污染,从而减少富营养化*;
  • 它们对温室气体(GHG)排放的平衡有积极影响,包括主要来自矿物肥料和动物粪便的CO2、N2O或氨(共生固定仅产生少量的N2O)。

  除了这些与共生存在直接相关的优势之外,豆科植物也有其所固有的优势,无论它们是否与根瘤菌建立了共生关系:

  • 通过建立菌根共生关系,它们可以去除土壤中的磷(限制植物生长的另一因素),并使其他植物物种更容易获得磷。
  • 它们对土壤有积极的影响(通过根系发育稳定、限制径流和侵蚀),对作物轮作有积极的影响(减少化肥使用、减少植物保护措施)。
  • 最后,作为一种天然肥料,它们通过提高植物物种的生产力、吸引传粉者(蜜蜂)和为作物辅助动物和大型动物(鸟类、哺乳动物)提供庇护所而对生物多样性产生积极影响

5. 作物组合,农业生态的解决方案

环境百科全书-靠空气生存的植物-组合栽培
图 10 组合栽培。A 左:谷物-野豌豆交替种植 B 中:有机混合谷物(黑小麦;大麦;燕麦)和豆类(豌豆)种植 C 右:简易农林系统,一种多年生木本植物行栽(橄榄树)和两种植物行下盖栽或固氮植物(紫花苜蓿)和行间粮食作物(硬粒小麦)组合栽培。[资料来源: A, Michel Gosselin
法国国家农业科学研究院媒体图书馆; B and C, Christophe Maître, 法国国家农业科学研究院媒体图书馆]

  在大规模农业区,法国农业受到作物轮作简化和增加投入(化肥)的显著影响。多样化的农业生态系统日益被认为是可持续发展的重要杠杆。谷物-豆科植物组合、共同播种和收获的模式,集中测试了地块内栽培多样性的提升(图10)。这些组合似乎使有机和传统农业在面对生物和非生物危害时能够应对来自生产、减少投入和作物的环境影响以及稳定方面的挑战[10]。在这种背景下,选择适合这些作物组合的品种成为一项重大挑战。

  与单一作物相比,谷类-豆类组合*作物提高了资源利用率。这尤其导致:

  • 比单一作物的平均产量更高的粮食/种子产量*,
  • 与单独种植豆科植物相比,杂草的生物量减少,
  • 与单独种植谷物相比,作物中的蛋白质含量更高。

  在不利条件下,作物组合的优点就更加突出:单独种植的每种作物或两种作物的产量低,或单独种植的谷物中蛋白质含量低。当氮限制作物时,组合作物尤其有益,并有助于稳定有机农业的产量。

  这些益处的实现与豆科植物在组合种植中的比例密切相关。因此,在草原上,放牧组合的最佳操作条件约为30%-40%饲料豆科饲料,割草组合的最佳操作条件为50%-70%。无论如何,豆科植物都可以成为推动作物转向可持续农业的驱动力。可持续农业尊重生态、经济和社会标准,以确保农业生产的长期发展。

6. 要点

  • 一些细菌能够利用大气中的氮来合成其生物分子(海洋蓝藻细菌,游离或与某些植物的根共生的土壤细菌):这就是氮的生物固定。
  • 在豆科植物中,共生细菌穿透根系并形成一个新的器官:结瘤。这个器官是将大气中的氮还原为氨的场所;它含有一种与动物肌红蛋白类似的蛋白质:豆血红蛋白。
  • 豆类富含蛋白质,是均衡的植物蛋白饮食中谷物蛋白质的极好补充。
  • 生物固氮的好处是多方面的:经济方面(节省氮肥)和环境方面(减少空气和地下水污染,促进可持续发展的作物组合)。

 


参考资料及说明

封面照片:[来源:©Marie-Christine Lhopital, 法国国家农业科学研究院媒体图书馆]

[1] 蔬菜和豆科植物不应该混淆。蔬菜(vegetable)来自拉丁语legumen,指的是果实为豆荚的植物(“legumen”的豆荚)。随后,legumen指所有的蔬菜植物种类。而且在目前的使用中,vegetable指一种可种植的植物,可食用的地方包括种类、叶子、根、块茎、果实、种子;vegetable也指植物可食用的部分。注意,在法语中,豆科植物被称为“légimineuses”。

[2] Ferguson BJ, Indrasumunar A, Hayashi S, Lin M-H, Lin Y-H, Reid DE, Gresshoff PM (2010). Molecular analysis of vegetable nodule development and autoregulation. Journal of Integrative Plant Biology, 52: 61-76.

[3] 括号中的数字为氮气循环图(图7)。

[4] 哈伯-博施法以氨的形式经济地固定大气中的氮,从而可以合成不同的炸药和氮肥。因此,从人口统计学的角度来看,它可能是20世纪最重要的工业过程。

[5] Erisman E, Sutton MA, Galloway J, Klimont Z, Winiwarter W (2008). How a century of ammonia synthesis changed the world. Nature Geoscience, 1: 636-639.

[6] Champ M, Magrini M-B, Simon N, Le Guillou C (2015). Les légumineuses pour l’alimentation humaines : apport nutritionnel et effets santé, usages et perspectives. In Les légumineuses pour des systèmes agricole et alimentaires durables, Schneider A & Huyghe C Coord., Editions Quae, pp 263-295. (法语)

[7] Tomé D (2012). Criteria and markers for protein quality assessment – a review. J. Nutr. 108 (S2): S222-229.

[8] Champ M, Anderson JW, Bach-Knudsen KE (2002). Supplement pulses and human health. J. Nutr, 88 (S3): S237-319.

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The Encyclopedia of the Environment by the Association des Encyclopédies de l'Environnement et de l'Énergie (www.a3e.fr), contractually linked to the University of Grenoble Alpes and Grenoble INP, and sponsored by the French Academy of Sciences.

To cite this article: BROUQUISSE Renaud, PUPPO Alain (March 11, 2024), 靠空气生存的植物, Encyclopedia of the Environment, Accessed November 1, 2024 [online ISSN 2555-0950] url : https://www.encyclopedie-environnement.org/zh/vivant-zh/plants-that-live-on-air/.

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